Splenic Responses in Ischemic Stroke: New Insights into Stroke Pathology

CNS Neuroscience and Therapeutics

Volumn 21, Issue 4, 2015, Pages 320-326

  Liu, Zong Jian ^a   Chen, Chen ^a   Li, Feng Wu ^a   Shen, Jia Mei ^a   Yang, Yuan Yuan ^b   Leak, Rehana K ^c   Ji, Xun Ming ^a,d   Du, Hui Shan ^a   Hu, Xiao Ming ^a,e  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c DUQUESNE UNIVERSITY   (United States)

^d CAPITAL MEDICAL UNIVERSITY   (China)

^e FUDAN UNIVERSITY   (China)

Author keywords

Immune response; Spleen; Stroke; Therapeutic strategies

Indexed keywords

AGMATINE; ANTIGEN; CATECHOLAMINE; CHEMOKINE RECEPTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; SIMVASTATIN;

AUTONOMIC NERVOUS SYSTEM; BRAIN DAMAGE; BRAIN INFARCTION; BRAIN ISCHEMIA; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR ACCIDENT; DENDRITIC CELL; DISEASE COURSE; GAMMA RADIATION; HUMAN; INFECTION; LYMPHOCYTE; MACROPHAGE; MONOCYTE; NATURAL KILLER CELL; NERVE DEGENERATION; NEUTROPHIL; NONHUMAN; POSTSTROKE INFECTION; RADIATION; REVIEW; SPLEEN; SPLEEN ATROPHY; SPLEEN DISEASE; STEM CELL TRANSPLANTATION; UMBILICAL CORD BLOOD; ANIMAL; BRAIN; CYTOLOGY; PATHOPHYSIOLOGY; STROKE;

ANIMALS; BRAIN; BRAIN ISCHEMIA; HUMANS; NERVE DEGENERATION; SPLEEN; STROKE;

EID: 84925361289     PISSN: 17555930     EISSN: 17555949     Source Type: Journal    
DOI: 10.1111/cns.12361     Document Type: Review

References (67)

1. Iadecola C, Anrather J. The immunology of stroke: From mechanisms to translation. Nat Med 2011;17:796-808.
2. Mebius RE, Kraal G. Structure and function of the spleen. Nat Rev Immunol 2005;5:606-616.
3. Offner H, Subramanian S, Parker SM, et al. Splenic atrophy in experimental stroke is accompanied by increased regulatory T cells and circulating macrophages. J Immunol 2006;176:6523-6531.
4. Ajmo CT Jr, Collier LA, Leonardo CC, et al. Blockade of adrenoreceptors inhibits the splenic response to stroke. Exp Neurol 2009;218:47-55.
5. Seifert HA, Hall AA, Chapman CB, et al. A transient decrease in spleen size following stroke corresponds to splenocyte release into systemic circulation. J Neuroimmune Pharmacol 2012;7:1017-1024.
6. Vendrame M, Gemma C, Pennypacker KR, et al. Cord blood rescues stroke-induced changes in splenocyte phenotype and function. Exp Neurol 2006;199:191-200.
7. Sahota P, Vahidy F, Nguyen C, et al. Changes in spleen size in patients with acute ischemic stroke: A pilot observational study. Int J Stroke 2013;8:60-67.
8. Prass K, Meisel C, Hoflich C, et al. Stroke-induced immunodeficiency promotes spontaneous bacterial infections and is mediated by sympathetic activation reversal by poststroke T helper cell type 1-like immunostimulation. J Exp Med 2003;198:725-736.
9. Li P, Gan Y, Sun BL, et al. Adoptive regulatory T-cell therapy protects against cerebral ischemia. Ann Neurol 2013;74:458-471.
10. Liesz A, Suri-Payer E, Veltkamp C, et al. Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke. Nat Med 2009;15:192-199.
11. Offner H, Subramanian S, Parker SM, et al. Experimental stroke induces massive, rapid activation of the peripheral immune system. J Cereb Blood Flow Metab 2006;26:654-665.
12. Seifert HA, Leonardo CC, Hall AA, et al. The spleen contributes to stroke induced neurodegeneration through interferon gamma signaling. Metab Brain Dis 2012;27:131-141.
13. Seifert HA, Collier LA, Chapman CB, et al. Pro-Inflammatory Interferon Gamma Signaling is Directly Associated with Stroke Induced Neurodegeneration. J Neuroimmune Pharmacol 2014;9:679-689.
14. Planas AM, Gomez-Choco M, Urra X, et al. Brain-derived antigens in lymphoid tissue of patients with acute stroke. J Immunol 2012;188:2156-2163.
15. Tsuchida T, Parker KC, Turner RV, et al. Autoreactive CD8+ T-cell responses to human myelin protein-derived peptides. Proc Natl Acad Sci U S A 1994;91:10859-10863.
16. Dimitrijevic OB, Stamatovic SM, Keep RF, Andjelkovic AV. Absence of the chemokine receptor CCR2 protects against cerebral ischemia/reperfusion injury in mice. Stroke 2007;38:1345-1353.
17. Bao Y, Kim E, Bhosle S, Mehta H, Cho S. A role for spleen monocytes in post-ischemic brain inflammation and injury. J Neuroinflammation 2010;7:92.
18. Hill WD, Hess DC, Martin-Studdard A, et al. SDF-1 (CXCL12) is upregulated in the ischemic penumbra following stroke: Association with bone marrow cell homing to injury. J Neuropathol Exp Neurol 2004;63:84-96.
19. Ruscher K, Kuric E, Liu Y, et al. Inhibition of CXCL12 signaling attenuates the postischemic immune response and improves functional recovery after stroke. J Cereb Blood Flow Metab 2013;33:1225-1234.
20. Kim JS, Gautam SC, Chopp M, et al. Expression of monocyte chemoattractant protein-1 and macrophage inflammatory protein-1 after focal cerebral ischemia in the rat. J Neuroimmunol 1995;56:127-134.
21. Reichel CA, Rehberg M, Lerchenberger M, et al. Ccl2 and Ccl3 mediate neutrophil recruitment via induction of protein synthesis and generation of lipid mediators. Arterioscler Thromb Vasc Biol 2009;29:1787-1793.
22. Terao S, Yilmaz G, Stokes KY, et al. Blood cell-derived RANTES mediates cerebral microvascular dysfunction, inflammation, and tissue injury after focal ischemia-reperfusion. Stroke 2008;39:2560-2570.
23. Bazan JF, Bacon KB, Hardiman G, et al. A new class of membrane-bound chemokine with a CX3C motif. Nature 1997;385:640-644.
24. Denes A, Ferenczi S, Halasz J, Kornyei Z, Kovacs KJ. Role of CX3CR1 (fractalkine receptor) in brain damage and inflammation induced by focal cerebral ischemia in mouse. J Cereb Blood Flow Metab 2008;28:1707-1721.
25. Gan Y, Liu Q, Wu W, et al. Ischemic neurons recruit natural killer cells that accelerate brain infarction. Proc Natl Acad Sci U S A 2014;111:2704-2709.
26. Domac FM, Misirli H. The role of neutrophils and interleukin-8 in acute ischemic stroke. Neurosciences (Riyadh) 2008;13:136-141.
27. Ay I, Sorensen AG, Ay H. Vagus nerve stimulation reduces infarct size in rat focal cerebral ischemia: An unlikely role for cerebral blood flow. Brain Res 2011;1392:110-115.
28. Rosas-Ballina M, Olofsson PS, Ochani M, et al. Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 2011;334:98-101.
29. Kohm AP, Sanders VM. Norepinephrine and beta 2-adrenergic receptor stimulation regulate CD4+ T and B lymphocyte function in vitro and in vivo. Pharmacol Rev 2001;53:487-525.
30. Mignini F, Streccioni V, Amenta F. Autonomic innervation of immune organs and neuroimmune modulation. Auton Autacoid Pharmacol 2003;23:1-25.
31. Arnon TI, Cyster JG. Blood, sphingosine-1-phosphate and lymphocyte migration dynamics in the spleen. Curr Top Microbiol Immunol 2014;378:107-128.
32. Kraft P, Gob E, Schuhmann MK, et al. FTY720 ameliorates acute ischemic stroke in mice by reducing thrombo-inflammation but not by direct neuroprotection. Stroke 2013;44:3202-3210.
33. An C, Shi Y, Li P, et al. Molecular dialogs between the ischemic brain and the peripheral immune system: Dualistic roles in injury and repair. Prog Neurobiol 2014;115:6-24.
34. Emsley HC, Smith CJ, Gavin CM, et al. An early and sustained peripheral inflammatory response in acute ischaemic stroke: Relationships with infection and atherosclerosis. J Neuroimmunol 2003;139:93-101.
35. Ostrowski RP, Schulte RW, Nie Y, et al. Acute splenic irradiation reduces brain injury in the rat focal ischemic stroke model. Transl Stroke Res 2012;3:473-481.
36. Kim E, Yang J, Beltran CD, Cho S. Role of spleen-derived monocytes/macrophages in acute ischemic brain injury. J Cereb Blood Flow Metab 2014;34:1411-1419.
37. Jin R, Yang G, Li G. Inflammatory mechanisms in ischemic stroke: Role of inflammatory cells. J Leukoc Biol 2010;87:779-789.
38. Price CJ, Menon DK, Peters AM, et al. Cerebral neutrophil recruitment, histology, and outcome in acute ischemic stroke: An imaging-based study. Stroke 2004;35:1659-1664.
39. Kim J, Song TJ, Park JH, et al. Different prognostic value of white blood cell subtypes in patients with acute cerebral infarction. Atherosclerosis 2012;222:464-467.
40. Ajmo CT Jr, Vernon DO, Collier L, et al. The spleen contributes to stroke-induced neurodegeneration. J Neurosci Res 2008;86:2227-2234.
41. Amantea D, Nappi G, Bernardi G, Bagetta G, Corasaniti MT. Post-ischemic brain damage: Pathophysiology and role of inflammatory mediators. FEBS J 2009;276:13-26.
42. Justicia C, Panes J, Sole S, et al. Neutrophil infiltration increases matrix metalloproteinase-9 in the ischemic brain after occlusion/reperfusion of the middle cerebral artery in rats. J Cereb Blood Flow Metab 2003;23:1430-1440.
43. Hurn PD, Subramanian S, Parker SM, et al. T- and B-cell-deficient mice with experimental stroke have reduced lesion size and inflammation. J Cereb Blood Flow Metab 2007;27:1798-1805.
44. Yilmaz G, Arumugam TV, Stokes KY, Granger DN. Role of T lymphocytes and interferon-gamma in ischemic stroke. Circulation 2006;113:2105-2112.
45. Zhang BJ, Men XJ, Lu ZQ, et al. Splenectomy protects experimental rats from cerebral damage after stroke due to anti-inflammatory effects. Chin Med J (Engl) 2013;126:2354-2360.
46. Bodhankar S, Chen Y, Vandenbark AA, Murphy SJ, Offner H. IL-10-producing B-cells limit CNS inflammation and infarct volume in experimental stroke. Metab Brain Dis 2013;28:375-386.
47. Zhang Y, Gao Z, Wang D, et al. Accumulation of natural killer cells in ischemic brain tissues and the chemotactic effect of IP-10. J Neuroinflammation 2014;11:79.
48. Gelderblom M, Leypoldt F, Steinbach K, et al. Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke 2009;40:1849-1857.
49. Alvarez D, Vollmann EH, von Andrian UH. Mechanisms and consequences of dendritic cell migration. Immunity 2008;29:325-342.
50. Banchereau J, Briere F, Caux C, et al. Immunobiology of dendritic cells. Annu Rev Immunol 2000;18:767-811.
51. Chen J, Sanberg PR, Li Y, et al. Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke 2001;32:2682-2688.
52. Vendrame M, Cassady J, Newcomb J, et al. Infusion of human umbilical cord blood cells in a rat model of stroke dose-dependently rescues behavioral deficits and reduces infarct volume. Stroke 2004;35:2390-2395.
53. Willing AE, Vendrame M, Mallery J, et al. Mobilized peripheral blood cells administered intravenously produce functional recovery in stroke. Cell Transplant 2003;12:449-454.
54. Vendrame M, Gemma C, de Mesquita D, et al. Anti-inflammatory effects of human cord blood cells in a rat model of stroke. Stem Cells Dev 2005;14:595-604.
55. Hao L, Zou Z, Tian H, et al. Stem cell-based therapies for ischemic stroke. Biomed Res Int 2014;2014:468748.
56. Yang M, Wei X, Li J, et al. Changes in host blood factors and brain glia accompanying the functional recovery after systemic administration of bone marrow stem cells in ischemic stroke rats. Cell Transplant 2010;19:1073-1084.
57. Takahashi A, Ohnishi K, Asakawa I, et al. Radiation response of apoptosis in C57BL/6N mouse spleen after whole-body irradiation. Int J Radiat Biol 2001;77:939-945.
58. Li G, Regunathan S, Barrow CJ, et al. Agmatine: An endogenous clonidine-displacing substance in the brain. Science 1994;263:966-969.
59. Uranchimeg D, Kim JH, Kim JY, et al. Recovered changes in the spleen by agmatine treatment after transient cerebral ischemia. Anat Cell Biol 2010;43:44-53.
60. Chen J, Zhang ZG, Li Y, et al. Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke. Ann Neurol 2003;53:743-751.
61. Zhang L, Zhang ZG, Ding GL, et al. Multitargeted effects of statin-enhanced thrombolytic therapy for stroke with recombinant human tissue-type plasminogen activator in the rat. Circulation 2005;112:3486-3494.
62. Cakmak A, Yemisci M, Koksoy C, et al. Statin pre-treatment protects brain against focal cerebral ischemia in diabetic mice. J Surg Res 2007;138:254-258.
63. Zacharek A, Chen J, Cui X, Yang Y, Chopp M. Simvastatin increases notch signaling activity and promotes arteriogenesis after stroke. Stroke 2009;40:254-260.
64. Tziomalos K, Giampatzis V, Bouziana SD, et al. Effect of prior treatment with different statins on stroke severity and functional outcome at discharge in patients with acute ischemic stroke. Int J Stroke 2013;8:E49.
65. Jain MK, Ridker PM. Anti-inflammatory effects of statins: Clinical evidence and basic mechanisms. Nat Rev Drug Discov 2005;4:977-987.
66. Jin R, Zhu X, Liu L, et al. Simvastatin attenuates stroke-induced splenic atrophy and lung susceptibility to spontaneous bacterial infection in mice. Stroke 2013;44:1135-1143.
67. Fathali N, Ostrowski RP, Hasegawa Y, et al. Splenic immune cells in experimental neonatal hypoxia-ischemia. Transl Stroke Res 2013;4:208-219.