Inflammation after Ischemic Stroke: The Role of Leukocytes and Glial Cells

다국어 초록 (Multilingual Abstract)

The immune response after stroke is known to play a major role in ischemic brain pathobiology. The inflammatory signals released by immune mediators activated by brain injury sets off a complex series of biochemical and molecular events which have been increasingly recognized as a key contributor to neuronal cell death. The primary immune mediators involved are glial cells and infiltrating leukocytes, including neutrophils, monocytes and lymphocyte. After ischemic stroke, activation of glial cells and subsequent release of pro- and anti-inflammatory signals are important for modulating both neuronal cell damage and wound healing. Infiltrated leukocytes release inflammatory mediators into the site of the lesion, thereby exacerbating brain injury. This review describes how the roles of glial cells and circulating leukocytes are a double-edged sword for neuroinflammation by focusing on their detrimental and protective effects in ischemic stroke. Here, we will focus on underlying characterize of glial cells and leukocytes under inflammation after ischemic stroke.

참고문헌 (Reference)

1 Geissmann F, "Unravelling mononuclear phagocyte heterogeneity" 10 : 453-460, 2010

2 Kawabori M, "Triggering receptor expressed on myeloid cells 2 (TREM2) deficiency attenuates phagocytic activities of microglia and exacerbates ischemic damage in experimental stroke" 35 : 3384-3396, 2015

3 Kumar A, "Traumatic brain injury in aged animals increases lesion size and chronically alters microglial/macrophage classical and alternative activation states" 34 : 1397-1411, 2013

4 Stevens SL, "The use of flow cytometry to evaluate temporal changes in inflammatory cells following focal cerebral ischemia in mice" 932 : 110-119, 2002

5 Kawabori M, "The role of the microglia in acute CNS injury" 30 : 381-392, 2015

6 Arvin B, "The role of inflammation and cytokines in brain injury" 20 : 445-452, 1996

7 DeGraba TJ, "The role of inflammation after acute stroke: utility of pursuing anti-adhesion molecule therapy" 51 : S62-S68, 1998

8 Schilling M, "The role of CC chemokine receptor 2 on microglia activation and blood-borne cell recruitment after transient focal cerebral ischemia in mice" 1289 : 79-84, 2009

9 Appel SH, "The microglial-motoneuron dialogue in ALS" 30 : 4-8, 2011

10 Villa P, "The interleukin-8 (IL-8/CXCL8) receptor inhibitor reparixin improves neurological deficits and reduces longterm inflammation in permanent and transient cerebral ischemia in rats" 13 : 125-133, 2007

11 Wang Q, "The inflammatory response in stroke" 184 : 53-68, 2007

12 Zhang R, "The expression of P- and E-selectins in three models of middle cerebral artery occlusion" 785 : 207-214, 1998

13 Mantovani A, "The chemokine system in diverse forms of macrophage activation and polarization" 25 : 677-686, 2004

14 Rossi D, "The biology of chemokines and their receptors" 18 : 217-242, 2000

15 Gelderblom M, "Temporal and spatial dynamics of cerebral immune cell accumulation in stroke" 40 : 1849-1857, 2009

16 Donohue PJ, "TWEAK is an endothelial cell growth and chemotactic factor that also potentiates FGF-2 and VEGF-A mitogenic activity" 23 : 594-600, 2003

17 Hurn PD, "T- and B-cell-deficient mice with experimental stroke have reduced lesion size and inflammation" 27 : 1798-1805, 2007

18 Nowicka D, "Spatiotemporal dynamics of astroglial and microglial responses after photothrombotic stroke in the rat brain" 68 : 155-168, 2008

19 Hallenbeck JM, "Significance of the inflammatory response in brain ischemia" 66 : 27-31, 1996

20 Zhao BQ, "Role of matrix metalloproteinases in delayed cortical responses after stroke" 12 : 441-445, 2006

21 Yilmaz G, "Role of T lymphocytes and interferon-gamma in ischemic stroke" 113 : 2105-2112, 2006

22 Chu HX, "Role of CCR2 in inflammatory conditions of the central nervous system" 34 : 1425-1429, 2014

23 Liesz A, "Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke" 15 : 192-199, 2009

24 Aisen PS, "Randomized pilot study of nimesulide treatment in Alzheimer's disease" 58 : 1050-1054, 2002

25 Sawada M, "Production of tumor necrosis factor-alpha by microglia and astrocytes in culture" 491 : 394-397, 1989

26 Suzuki H, "Postischemic expression of P-selectin immunoreactivity in rat brain" 228 : 151-154, 1997

27 Huang J, "Postischemic cerebrovascular E-selectin expression mediates tissue injury in murine stroke" 31 : 3047-3053, 2000

28 Shichita T, "Pivotal role of cerebral interleukin-17-producing gammadeltaT cells in the delayed phase of ischemic brain injury" 15 : 946-950, 2009

29 Carlin LM, "Nr4a1-dependent Ly6C(low) monocytes monitor endothelial cells and orchestrate their disposal" 153 : 362-375, 2013

30 Nair MG, "Novel effector molecules in type 2 inflammation: lessons drawn from helminth infection and allergy" 177 : 1393-1399, 2006

31 Bargatze RF, "Neutrophils roll on adherent neutrophils bound to cytokineinduced endothelial cells via L-selectin on the rolling cells" 180 : 1785-1792, 1994

32 Dimasi D, "Neutrophil interactions with the vascular endothelium" 17 : 1167-1175, 2013

33 Dinkel K, "Neurotoxic effects of polymorphonuclear granulocytes on hippocampal primary cultures" 101 : 331-336, 2004

34 Ren X, "Myelin specific cells infiltrate MCAO lesions and exacerbate stroke severity" 27 : 7-15, 2012

35 Ginhoux F, "Monocytes and macrophages:developmental pathways and tissue homeostasis" 14 : 392-404, 2014

36 Gordon S, "Monocyte and macrophage heterogeneity" 5 : 953-964, 2005

37 Saijo K, "Microglial cell origin and phenotypes in health and disease" 11 : 775-787, 2011

38 Hanisch UK, "Microglia: active sensor and versatile effector cells in the normal and pathologic brain" 10 : 1387-1394, 2007

39 Kreutzberg GW, "Microglia: a sensor for pathological events in the CNS" 19 : 312-318, 1996

40 Hu X, "Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia" 43 : 3063-3070, 2012

41 Wang G, "Microglia/macrophage polarization dynamics in white matter after traumatic brain injury" 33 : 1864-1874, 2013

42 El Khour y J, "Microglia, scavenger receptors, and the pathogenesis of Alzheimer's disease" 19 : S81-S84, 1998

43 Lai AY, "Microglia in cerebral ischemia:molecular actions and interactions" 84 : 49-59, 2006

44 Soriano SG, "Mice deficient in Mac-1 (CD11b/CD18) are less susceptible to cerebral ischemia/reperfusion injury" 30 : 134-139, 1999

45 Brait VH, "Mechanisms contributing to cerebral infarct size after stroke: gender, reperfusion, T lymphocytes, and Nox2-derived superoxide" 30 : 1306-1317, 2010

46 Gliem M, "Macrophages prevent hemorrhagic infarct transformation in murine stroke models" 71 : 743-752, 2012

47 Lee SC, "Macrophage colony-stimulating factor in human fetal astrocytes and microglia. Differential regulation by cytokines and lipopolysaccharide, and modulation of class II MHC on microglia" 150 : 594-604, 1993

48 Yu Z, "MSX3 switches microglia polarization and protects from inflammationinduced demyelination" 35 : 6350-6365, 2015

49 Mittelbronn M, "Local distribution of microglia in the normal adult human central nervous system differs by up to one order of magnitude" 101 : 249-255, 2001

50 Kataoka H, "Leukocyteendothelium interactions during permanent focal cerebral ischemia in mice" 24 : 668-676, 2004

51 Panés J, "Leukocyte-endothelial cell adhesion: avenues for therapeutic intervention" 126 : 537-550, 1999

52 Harrison DG, "Is hypertension an immunologic disease?" 10 : 464-469, 2008

53 Kim JY, "Innate inflammatory responses in stroke: mechanisms and potential therapeutic targets" 21 : 2076-2097, 2014

54 Yu YM, "Inhibition of the cerebral ischemic injury by ethyl pyruvate with a wide therapeutic window" 36 : 2238-2243, 2005

55 Liesz A, "Inhibition of lymphocyte trafficking shields the brain against deleterious neuroinflammation after stroke" 134 : 704-720, 2011

56 Vemuganti R, "Inhibition of intercellular adhesion molecule-1 protein expression by antisense oligonucleotides is neuroprotective after transient middle cerebral artery occlusion in rat" 35 : 179-184, 2004

57 Danton GH, "Inflammatory mechanisms after ischemia and stroke" 62 : 127-136, 2003

58 Tuttolomondo A, "Inflammatory cytokines in acute ischemic stroke" 14 : 3574-3589, 2008

59 Kriz J, "Inflammation in ischemic brain injury: timing is important" 18 : 145-157, 2006

60 Emsley HC, "Inflammation and infection in clinical stroke" 22 : 1399-1419, 2002

61 Becker KJ, "Inflammation and acute stroke" 11 : 45-49, 1998

62 Garcia-Bonilla L, "Inducible nitric oxide synthase in neutrophils and endothelium contributes to ischemic brain injury in mice" 193 : 2531-2537, 2014

63 Wang X, "Induced expression of adhesion molecules following focal brain ischemia" 12 : 825-832, 1995

64 Stanimirovic DB, "Increase in surface expression of ICAM-1, VCAM-1 and E-selectin in human cerebromicrovascular endothelial cells subjected to ischemia-like insults" 70 : 12-16, 1997

65 Hallenbeck JM, "Immunology of ischemic vascular disease: plaque to attack" 26 : 550-556, 2005

66 Saino O, "Immunodeficiency reduces neural stem/progenitor cell apoptosis and enhances neurogenesis in the cerebral cortex after stroke" 88 : 2385-2397, 2010

67 Dong Y, "Immune function of astrocytes" 36 : 180-190, 2001

68 Yenari MA, "Hu23F2G, an antibody recognizing the leukocyte CD11/CD18 integrin, reduces injury in a rabbit model of transient focal cerebral ischemia" 153 : 223-233, 1998

69 Colton CA, "Heterogeneity of microglial activation in the innate immune response in the brain" 4 : 399-418, 2009

70 Wong CH, "Functional innervation of hepatic iNKT cells is immunosuppressive following stroke" 334 : 101-105, 2011

71 Ritzel RM, "Functional differences between microglia and monocytes after ischemic stroke" 12 : 106-, 2015

72 Salemi J, "Flipping the switches:CD40 and CD45 modulation of microglial activation states in HIV associated dementia (HAD)" 6 : 3-, 2011

73 Endoh M, "Expression of the inducible form of nitric oxide synthase by reactive astrocytes after transient global ischemia" 651 : 92-100, 1994

74 Kim JS, "Expression of monocyte chemoattractant protein-1 and macrophage inflammatory protein-1 after focal cerebral ischemia in the rat" 56 : 127-134, 1995

75 Li GZ, "Expression of interleukin-17 in ischemic brain tissue" 62 : 481-486, 2005

76 Mosser DM, "Exploring the full spectrum of macrophage activation" 8 : 958-969, 2008

77 Härtl R, "Experimental antileukocyte interventions in cerebral ischemia" 16 : 1108-1119, 1996

78 Zhang L, "Effects of a selective CD11b/CD18 antagonist and recombinant human tissue plasminogen activator treatment alone and in combination in a rat embolic model of stroke" 34 : 1790-1795, 2003

79 Kleinschnitz C, "Early detrimental T-cell effects in experimental cerebral ischemia are neither related to adaptive immunity nor thrombus formation" 115 : 3835-3842, 2010

80 Bizzarri C, "ELR+ CXC chemokines and their receptors (CXC chemokine receptor 1 and CXC chemokine receptor 2) as new therapeutic targets" 112 : 139-149, 2006

81 Wendy C. Huang, "Direct protection of cultured neurons from ischemia-like injury by minocycline" 대한해부학회 43 (43): 325-331, 2011

82 Geissmann F, "Development of monocytes, macrophages, and dendritic cells" 327 : 656-661, 2010

83 Barry M, "Cytotoxic T lymphocytes: all roads lead to death" 2 : 401-409, 2002

84 Kim JS, "Cytokines and adhesion molecules in stroke and related diseases" 137 : 69-78, 1996

85 Benveniste EN, "Cytokine actions in the central nervous system" 9 : 259-275, 1998

86 Chawla A, "Control of macrophage activation and function by PPARs" 106 : 1559-1569, 2010

87 Gerard C, "Chemokines and disease" 2 : 108-115, 2001

88 Brait VH, "Chemokine-related gene expression in the brain following ischemic stroke: no role for CXCR2 in outcome" 1372 : 169-179, 2011

89 Khan M, "Cerebrovascular protection by various nitric oxide donors in rats after experimental stroke" 15 : 114-124, 2006

90 Iadecola C, "Cerebral ischemia and inflammation" 14 : 89-94, 2001

91 Yilmaz G, "Cell adhesion molecules and ischemic stroke" 30 : 783-793, 2008

92 Schubert P, "Cascading glia reactions: a common pathomechanism and its differentiated control by cyclic nucleotide signaling" 903 : 24-33, 2000

93 Morganti JM, "Call off the dog(ma):M1/M2 polarization is concurrent following traumatic brain injury" 11 : e0148001-, 2016

94 Auffray C, "Blood monocytes: development, heterogeneity, and relationship with dendritic cells" 27 : 669-692, 2009

95 Piccio L, "Blockade of TREM-2 exacerbates experimental autoimmune encephalomyelitis" 37 : 1290-1301, 2007

96 Anderson MA, "Astrocyte scar formation aids central nervous system axon regeneration" 532 : 195-200, 2016

97 Pekny M, "Astrocyte activation and reactive gliosis" 50 : 427-434, 2005

98 Becker K, "Antibody to the alpha4 integrin decreases infarct size in transient focal cerebral ischemia in rats" 32 : 206-211, 2001

99 Chopp M, "Antibodies against adhesion molecules reduce apoptosis after transient middle cerebral artery occlusion in rat brain" 16 : 578-584, 1996

100 Nguyen KD, "Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis" 480 : 104-108, 2011

101 Peferoen LA, "Activation status of human microglia is dependent on lesion formation stage and remyelination in multiple sclerosis" 74 : 48-63, 2015

102 Lehnardt S, "Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway" 100 : 8514-8519, 2003

103 Dimitrijevic OB, "Absence of the chemokine receptor CCR2 protects against cerebral ischemia/reperfusion injury in mice" 38 : 1345-1353, 2007

104 Yepes M, "A soluble Fn14-Fc decoy receptor reduces infarct volume in a murine model of cerebral ischemia" 166 : 511-520, 2005

105 Hsieh CL, "A role for TREM2ligands in the phagocytosis of apoptotic neuronal cells by microglia" 109 : 1144-1156, 2009

106 Naert G, "A deficiency in CCR2+ monocytes:the hidden side of Alzheimer's disease" 5 : 284-293, 2013