Depletion of microglia exacerbates postischemic inflammation and brain injury

Journal of Cerebral Blood Flow and Metabolism

Volumn 37, Issue 6, 2017, Pages 2224-2236

  Jin, Wei Na ^a,b   Shi, Samuel Xiang Yu ^b,c   Li, Zhiguo ^a,b   Li, Minshu ^a,b   Wood, Kristofer ^b   Gonzales, Rayna J ^c   Liu, Qiang ^a,b  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b BARROW NEUROLOGICAL INSTITUTE   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Brain ischemia; Colony stimulating factor 1 receptor; Microglia; Neuroprotection

Indexed keywords

AGENTS AFFECTING METABOLISM; BINDARIT; COLONY STIMULATING FACTOR 1; GLUCOSE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; LACTATE DEHYDROGENASE; MONOCYTE CHEMOTACTIC PROTEIN 1; OXYGEN; PLX 3397; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN C; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; 5-((5-CHLORO-1H-PYRROLO(2,3-B)PYRIDIN-3-YL)METHYL)-N-((6-(TRIFLUOROMETHYL)PYRIDIN-3-YL)METHYL)PYRIDIN-2-AMINE; AMINOPYRIDINE DERIVATIVE; AUTACOID; CSF1R PROTEIN, MOUSE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR RECEPTOR; PYRROLE DERIVATIVE; STEM CELL FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN METABOLISM; CELL DEATH; CELL INFILTRATION; CONTROLLED STUDY; DEPLETION; DISEASE EXACERBATION; ENCEPHALITIS; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; LEUKOCYTE; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROLOGIC EXAMINATION; NEUROPROTECTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIMARY CELL CULTURE; PRIORITY JOURNAL; REPERFUSION; TRANSIENT ISCHEMIC ATTACK; TUNEL ASSAY; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; DIAGNOSTIC IMAGING; DISEASE MODEL; IMMUNOLOGY; METABOLISM; NERVE CELL; PATHOLOGY;

AMINOPYRIDINES; ANIMALS; BRAIN ISCHEMIA; CELLS, CULTURED; DISEASE MODELS, ANIMAL; INFLAMMATION MEDIATORS; MAGNETIC RESONANCE IMAGING; MALE; MICE, INBRED C57BL; MICROGLIA; NEURONS; PRIMARY CELL CULTURE; PROTO-ONCOGENE PROTEINS C-KIT; PYRROLES; REACTIVE OXYGEN SPECIES; RECEPTORS, GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR;

EID: 85019689599     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1177/0271678X17694185     Document Type: Article

References (66)

1. Iadecola C, Anrather J. The immunology of stroke: From mechanisms to translation. Nat Med 2011; 17: 796–808.
2. Prabhakaran S, Ruff I, Bernstein RA. Acute stroke intervention: A systematic review. JAMA 2015; 313: 1451–1462.
3. Eltzschig HK, Eckle T. Ischemia and reperfusion – From mechanism to translation. Nat Med 2011; 17: 1391–1401.
4. Chamorro A, Meisel A, Planas AM, et al. The immunology of acute stroke. Nat Rev Neurol 2012; 8: 401–410.
5. Fu Y, Liu Q, Anrather J, et al. Immune interventions in stroke. Nat Rev Neurol 2015; 11: 524–535.
6. Keep RF, Hua Y, Xi G. Intracerebral haemorrhage: Mechanisms of injury and therapeutic targets. Lancet Neurol 2012; 11: 720–731.
7. Mracsko E, Veltkamp R. Neuroinflammation after intracerebral hemorrhage. Front Cell Neurosci 2014; 8: 388.
8. Macrez R, Ali C, Toutirais O, et al. Stroke and the immune system: From pathophysiology to new therapeutic strategies. Lancet Neurol 2011; 10: 471–480.
9. Taylor RA, Sansing LH. Microglial responses after ischemic stroke and intracerebral hemorrhage. Clin Develop Immunol 2013; 2013: 746068.
10. Wang YC, Zhou Y, Fang H, et al. Toll-like receptor 2/4 heterodimer mediates inflammatory injury in intracerebral hemorrhage. Ann Neurol 2014; 75: 876–889.
11. Wu J, Yang S, Xi G, et al. Microglial activation and brain injury after intracerebral hemorrhage. Acta Neurochir Suppl 2008; 105: 59–65.
12. Wang J, Rogove AD, Tsirka AE, et al. Protective role of tuftsin fragment 1-3 in an animal model of intracerebral hemorrhage. Ann Neurol 2003; 54: 655–664.
13. Hu X, Leak RK, Shi Y, et al. Microglial and macrophage polarization-new prospects for brain repair. Nat Rev Neurol 2015; 11: 56–64.
14. Ponomarev ED, Maresz K, Tan Y, et al. Cns-derived interleukin-4 is essential for the regulation of autoimmune inflammation and induces a state of alternative activation in microglial cells. J Neurosci 2007; 27: 10714–10721.
15. Kanazawa M, Kawamura K, Takahashi T, et al. Multiple therapeutic effects of progranulin on experimental acute ischaemic stroke. Brain 2015; 138: 1932–1948.
16. Sawano T, Watanabe F, Ishiguchi M, et al. Effect of sema4d on microglial function in middle cerebral artery occlusion mice. Glia 2015; 63: 2249–2259.
17. Shigemoto-Mogami Y, Hoshikawa K, Goldman JE, et al. Microglia enhance neurogenesis and oligodendrogenesis in the early postnatal subventricular zone. J Neurosci 2014; 34: 2231–2243.
18. Lalancette-Hebert M, Gowing G, Simard A, et al. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 2007; 27: 2596–2605.
19. Franco EC, Cardoso MM, Gouveia A, et al. Modulation of microglial activation enhances neuroprotection and functional recovery derived from bone marrow mononuclear cell transplantation after cortical ischemia. Neurosci Res 2012; 73: 122–132.
20. Faustino JV, Wang X, Johnson CE, et al. Microglial cells contribute to endogenous brain defenses after acute neonatal focal stroke. J Neurosci 2011; 31: 12992–13001.
21. Gehrmann J, Bonnekoh P, Miyazawa T, et al. Immunocytochemical study of an early microglial activation in ischemia. J Cereb Blood Flow Metab 1992; 12: 257–269.
22. Gelderblom M, Leypoldt F, Steinbach K, et al. Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke 2009; 40: 1849–1857.
23. Chen YJ, Nguyen HM, Maezawa I, et al, et al. The potassium channel kca3.1 constitutes a pharmacological target for neuroinflammation associated with ischemia/reperfusion stroke. J Cereb Blood Flow Metab 2016; 36: 2146–2161
24. Ortega FJ, Jolkkonen J, Rodriguez MJ. Microglia is an active player in how glibenclamide improves stroke outcome. J Cereb Blood Flow Metab 2013; 33: 1138–1139.
25. Colombo E, Farina C. Astrocytes: Key regulators of neuroinflammation. Trends Immunol 2016; 37: 608–620.
26. Kimelberg HK. Functions of mature mammalian astrocytes: A current view. Neuroscientist 2010; 16: 79–106.
27. Constantinescu CS, Tani M, Ransohoff RM, et al. Astrocytes as antigen-presenting cells: Expression of il-12/il-23. J Neurochem 2005; 95: 331–340.
28. Sofroniew MV. Astrocyte barriers to neurotoxic inflammation. Nat Rev Neurosci 2015; 16: 249–263.
29. Liu Z and Chopp M. Astrocytes, therapeutic targets for neuroprotection and neurorestoration in ischemic stroke. Prog Neurobiology 2016; 144: 103–120
30. Wang W, Redecker C, Yu ZY, et al. Rat focal cerebral ischemia induced astrocyte proliferation and delayed neuronal death are attenuated by cyclin-dependent kinase inhibition. J Clin Neurosci 2008; 15: 278–285.
31. Fang SH, Wei EQ, Zhou Y, et al. Increased expression of cysteinyl leukotriene receptor-1 in the brain mediates neuronal damage and astrogliosis after focal cerebral ischemia in rats. Neuroscience 2006; 140: 969–979.
32. Forslin Aronsson S, Spulber S, Popescu LM, et al. Alpha-melanocyte-stimulating hormone is neuroprotective in rat global cerebral ischemia. Neuropeptides 2006; 40: 65–75.
33. Ye YL, Shi WZ, Zhang WP, et al. Cilostazol, a phosphodiesterase 3 inhibitor, protects mice against acute and late ischemic brain injuries. Eur J Pharmacol 2007; 557: 23–31.
34. Elmore MR, Najafi AR, Koike MA, et al. Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron 2014; 82: 380–397.
35. Dagher NN, Najafi AR, Kayala KM, et al. Colony-stimulating factor 1 receptor inhibition prevents microglial plaque association and improves cognition in 3xtg-ad mice. J Neuroinflammation 2015; 12: 139.
36. Patel S, Player MR. Colony-stimulating factor-1 receptor inhibitors for the treatment of cancer and inflammatory disease. Curr Topics Med Chem 2009; 9: 599–610.
37. Erblich B, Zhu L, Etgen AM, et al. Absence of colony stimulation factor-1 receptor results in loss of microglia, disrupted brain development and olfactory deficits. PLoS One 2011; 6: e26317.
38. Nandi S, Gokhan S, Dai XM, et al. The csf-1 receptor ligands il-34 and csf-1 exhibit distinct developmental brain expression patterns and regulate neural progenitor cell maintenance and maturation. Dev Biol 2012; 367: 100–113.
39. Szalay G, Martinecz B, Lenart N, et al. Microglia protect against brain injury and their selective elimination dysregulates neuronal network activity after stroke. Nat Commun 2016; 7: 11499.
40. 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.
41. Liu Q, Tang Z, Gan Y, et al. Genetic deficiency of beta2-containing nicotinic receptors attenuates brain injury in ischemic stroke. Neuroscience 2014; 256: 170–177.
42. Tang Z, Gan Y, Liu Q, et al. Cx3cr1 deficiency suppresses activation and neurotoxicity of microglia/macrophage in experimental ischemic stroke. J Neuroinflammation 2014; 11: 26.
43. Jin WN, Yang X, Li Z, et al, et al. Non-invasive tracking of cd4+ t cells with a paramagnetic and fluorescent nanoparticle in brain ischemia. J Cereb Blood Flow Metab 2016; 36: 1464–1476
44. Hao J, Liu R, Piao W, et al. Central nervous system (cns)-resident natural killer cells suppress th17 responses and cns autoimmune pathology. J Exp Med 2010; 207: 1907–1921.
45. Hua Y, Xi G, Keep RF, et al. Plasminogen activator inhibitor-1 induction after experimental intracerebral hemorrhage. J Cereb Blood Flow Metab 2002; 22: 55–61.
46. Liu Q, Sanai N, Jin WN, et al. Neural stem cells sustain natural killer cells that dictate recovery from brain inflammation. Nat Neurosci 2016; 19: 243–252.
47. Bell JC, Liu Q, Gan Y, et al. Visualization of inflammation and demyelination in 2d2 transgenic mice with rodent MRI. J Neuroimmunol 2013; 264: 35–40.
48. Khan P, Idrees D, Moxley MA, et al. Luminol-based chemiluminescent signals: Clinical and non-clinical application and future uses. Appl Biochem Biotechnol 2014; 173: 333–355.
49. Shi FD, Van Kaer L. Reciprocal regulation between natural killer cells and autoreactive t cells. Nat Rev Immunol 2006; 6: 751–760.
50. Liu Q, Xie X, Lukas RJ, et al. A novel nicotinic mechanism underlies beta-amyloid-induced neuronal hyperexcitation. J Neurosci 2013; 33: 7253–7263.
51. Hopkins J, Hwang G, Jacob J, et al. Meiosis-specific cohesin component, stag3 is essential for maintaining centromere chromatid cohesion, and required for DNA repair and synapsis between homologous chromosomes. PLoS Genet 2014; 10: e1004413.
52. 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.
53. 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.
54. Mora E, Guglielmotti A, Biondi G, et al. Bindarit: An anti-inflammatory small molecule that modulates the nfkappab pathway. Cell Cycle 2012; 11: 159–169.
55. Ma Y, Wang J, Wang Y, et al, et al. The biphasic function of microglia in ischemic stroke. Prog Neurobiol. Epub ahead of print 2 February 2016. DOI: S0301-0082(15)30070-8
56. Hoehn BD, Palmer TD, Steinberg GK. Neurogenesis in rats after focal cerebral ischemia is enhanced by indomethacin. Stroke 2005; 36: 2718–2724.
57. Rice RA, Spangenberg EE, Yamate-Morgan H, et al. Elimination of microglia improves functional outcomes following extensive neuronal loss in the hippocampus. J Neurosci 2015; 35: 9977–9989.
58. Lambertsen KL, Clausen BH, Babcock AA, et al. Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neurosci 2009; 29: 1319–1330.
59. Shindo A, Maki T, Mandeville ET, et al. Astrocyte-derived pentraxin 3 supports blood-brain barrier integrity under acute phase of stroke. Stroke 2016; 47: 1094–1100.
60. Morken TS, Brekke E, Haberg A, et al. Altered astrocyte-neuronal interactions after hypoxia-ischemia in the neonatal brain in female and male rats. Stroke 2014; 45: 2777–2785.
61. Tsai HH, Li H, Fuentealba LC, et al. Regional astrocyte allocation regulates cns synaptogenesis and repair. Science 2012; 337: 358–362.
62. Nedergaard M, Dirnagl U. Role of glial cells in cerebral ischemia. Glia 2005; 50: 281–286.
63. Pascual O, Ben Achour S, Rostaing P, et al. Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc Natl Acad Sci U S A 2012; 109: E197–E205.
64. Shinozaki Y, Nomura M, Iwatsuki K, et al. Microglia trigger astrocyte-mediated neuroprotection via purinergic gliotransmission. Sci Rep 2014; 4: 4329.
65. Sherr CJ, Rettenmier CW, Sacca R, et al. The c-fms proto-oncogene product is related to the receptor for the mononuclear phagocyte growth factor, csf-1. Cell 1985; 41: 665–676.
66. Luo J, Elwood F, Britschgi M, et al. Colony-stimulating factor 1 receptor (csf1r) signaling in injured neurons facilitates protection and survival. J Exp Med 2013; 210: 157–172.