Role for microglia in sex differences after ischemic stroke: importance of M2

Metabolic Brain Disease

Volumn 30, Issue 6, 2015, Pages 1515-1529

  Bodhankar, Sheetal ^a,b   Lapato, Andrew ^a,b   Chen, Yingxin ^b   Vandenbark, Arthur A ^a,b   Saugstad, Julie A ^b,c   Offner, Halina ^a,b  

^a PORTLAND VA MEDICAL CENTER   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

IL 10 secreting B cells; M1 and M2 MG states; MCAO; Microglia

Indexed keywords

B7 ANTIGEN; CD11B ANTIGEN; CD206 ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CX3CR1; GLYCOPROTEIN P 15095; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR ALPHA; LYMPHOCYTE ANTIGEN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MESSENGER RNA; RECOMBINANT INTERLEUKIN 10; RECOMBINANT INTERLEUKIN 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; IL10 PROTEIN, MOUSE; LECTIN; MANNOSE BINDING LECTIN; MANNOSE RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BRAIN ISCHEMIA; CELL ACTIVATION; CELL INTERACTION; CELL SURFACE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; GLIAL CELL CULTURE; IMMUNOREGULATION; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; SEX DIFFERENCE; UPREGULATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL COMMUNICATION; CEREBRAL ARTERY DISEASE; CEREBROVASCULAR ACCIDENT; COCULTURE; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY; SEXUAL DEVELOPMENT;

ANIMALS; B-LYMPHOCYTES; BRAIN ISCHEMIA; CELL COMMUNICATION; COCULTURE TECHNIQUES; FEMALE; INFARCTION, MIDDLE CEREBRAL ARTERY; INTERLEUKIN-10; INTERLEUKIN-4; LECTINS, C-TYPE; MALE; MANNOSE-BINDING LECTINS; MICE; MICE, INBRED C57BL; MICROGLIA; RECEPTORS, CELL SURFACE; SEX CHARACTERISTICS; STROKE;

EID: 84947031340     PISSN: 08857490     EISSN: 15737365     Source Type: Journal    
DOI: 10.1007/s11011-015-9714-9     Document Type: Article

References (70)

1. Alkayed NJ, Harukuni I, Kimes AS, London ED, Traystman RJ, Hurn PD (1998) Gender-linked brain injury in experimental stroke. Stroke 29:159–165, discussion 166
2. Allan SM, Tyrrell PJ, Rothwell NJ (2005) Interleukin-1 and neuronal injury. Nat Rev Immunol 5:629–640. doi:10.1038/nri1664
3. Banerjee A, Wang J, Bodhankar S, Vandenbark AA, Murphy SJ, Offner H (2013) Phenotypic changes in immune cell subsets reflect increased infarct volume in male vs. female mice. Transl Stroke Res 4:554–563. doi:10.1007/s12975-013-0268-z
4. Boche D, Perry VH, Nicoll JA (2013) Review: activation patterns of microglia and their identification in the human brain. Neuropathol Appl Neurobiol 39:3–18. doi:10.1111/nan.12011
5. Bodhankar S, Chen Y, Vandenbark AA, Murphy SJ, Offner H (2013) IL-10-producing B-cells limit CNS inflammation and infarct volume in experimental stroke. Metab Brain Dis 28:375–386. doi:10.1007/s11011-013-9413-3
6. Bodhankar S, Chen Y, Lapato A, Vandenbark AA, Murphy SJ, Saugstad JA, Offner H (2014a) Regulatory CD8CD122 T-cells predominate in CNS after treatment of experimental stroke in male mice with IL-10-secreting B-cells. Metab Brain Dis. doi:10.1007/s11011-014-9639-8
7. Bodhankar S, Chen Y, Vandenbark AA, Murphy SJ, Offner H (2014b) Treatment of experimental stroke with IL-10-producing B-cells reduces infarct size and peripheral and CNS inflammation in wild-type B-cell-sufficient mice. Metab Brain Dis 29:59–73. doi:10.1007/s11011-013-9474-3
8. Butovsky O et al (2006a) Induction and blockage of oligodendrogenesis by differently activated microglia in an animal model of multiple sclerosis. J Clin Invest 116:905–915. doi:10.1172/JCI26836
9. Butovsky O et al (2006b) Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 31:149–160. doi:10.1016/j.mcn.2005.10.006
10. Cherry JD, Olschowka JA, O’Banion MK (2014) Neuroinflammation and M2 microglia: the good, the bad, and the inflamed. J Neuroinflammation 11:98. doi:10.1186/1742-2094-11-98
11. Chu M et al (2012) Focal cerebral ischemia activates neurovascular restorative dynamics in mouse brain. Front Biosci (Elite Ed) 4:1926–1936
12. de Bilbao F, Arsenijevic D, Moll T, Garcia-Gabay I, Vallet P, Langhans W, Giannakopoulos P (2009) In vivo over-expression of interleukin-10 increases resistance to focal brain ischemia in mice. J Neurochem 110:12–22. doi:10.1111/j.1471-4159.2009.06098.x
13. Denes A, Ferenczi S, Halasz J, Kornyei Z, Kovacs KJ (2008) Role of CX3CR1 (fractalkine receptor) in brain damage and inflammation induced by focal cerebral ischemia in mouse. J Cereb Blood Flow Metab 28:1707–1721. doi:10.1038/jcbfm.2008.64
14. Denker SP, Ji S, Dingman A, Lee SY, Derugin N, Wendland MF, Vexler ZS (2007) Macrophages are comprised of resident brain microglia not infiltrating peripheral monocytes acutely after neonatal stroke. J Neurochem 100:893–904. doi:10.1111/j.1471-4159.2006.04162.x
15. Draheim HJ, Prinz M, Weber JR, Weiser T, Kettenmann H, Hanisch UK (1999) Induction of potassium channels in mouse brain microglia: cells acquire responsiveness to pneumococcal cell wall components during late development. Neuroscience 89:1379–1390
16. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci U S A 100:13632–13637. doi:10.1073/pnas.2234031100
17. Floden AM, Combs CK (2007) Microglia repetitively isolated from in vitro mixed glial cultures retain their initial phenotype. J Neurosci Methods 164:218–224. doi:10.1016/j.jneumeth.2007.04.018
18. Fumagalli S, Perego C, Ortolano F, De Simoni MG (2013) CX3CR1 deficiency induces an early protective inflammatory environment in ischemic mice. Glia 61:827–842. doi:10.1002/glia.22474
19. Gadani SP, Cronk JC, Norris GT, Kipnis J (2012) IL-4 in the brain: a cytokine to remember. J Immunol 189:4213–4219. doi:10.4049/jimmunol.1202246
20. Gingras M, Gagnon V, Minotti S, Durham HD, Berthod F (2007) Optimized protocols for isolation of primary motor neurons, astrocytes and microglia from embryonic mouse spinal cord. J Neurosci Methods 163:111–118. doi:10.1016/j.jneumeth.2007.02.024
21. Giulian D, Baker TJ (1986) Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci 6:2163–2178
22. Gregersen R, Lambertsen K, Finsen B (2000) Microglia and macrophages are the major source of tumor necrosis factor in permanent middle cerebral artery occlusion in mice. J Cereb Blood Flow Metab 20:53–65. doi:10.1097/00004647-200001000-00009
23. Hallenbeck JM (2002) The many faces of tumor necrosis factor in stroke. Nat Med 8:1363–1368. doi:10.1038/nm1202-1363
24. Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387–1394. doi:10.1038/nn1997
25. Heyen JR, Ye S, Finck BN, Johnson RW (2000) Interleukin (IL)-10 inhibits IL-6 production in microglia by preventing activation of NF-kappaB. Brain Res Mol Brain Res 77:138–147
26. Horvath RJ, Nutile-McMenemy N, Alkaitis MS, Deleo JA (2008) Differential migration, LPS-induced cytokine, chemokine, and NO expression in immortalized BV-2 and HAPI cell lines and primary microglial cultures. J Neurochem 107:557–569. doi:10.1111/j.1471-4159.2008.05633.x
27. Hu X et al (2012) Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke 43:3063–3070. doi:10.1161/STROKEAHA.112.659656
28. Hu X, Leak RK, Shi Y, Suenaga J, Gao Y, Zheng P, Chen J (2015) Microglial and macrophage polarization-new prospects for brain repair. Nat Rev Neurol 11:56–64. doi:10.1038/nrneurol.2014.207
29. Jalal FY, Yang Y, Thompson J, Lopez AC, Rosenberg GA (2012) Myelin loss associated with neuroinflammation in hypertensive rats. Stroke 43:1115–1122. doi:10.1161/STROKEAHA.111.643080
30. Kelley KW, Bluthe RM, Dantzer R, Zhou JH, Shen WH, Johnson RW, Broussard SR (2003) Cytokine-induced sickness behavior. Brain Behav Immun 17(1):S112–S118
31. Kissela B et al (2009) Clinical prediction of functional outcome after ischemic stroke: the surprising importance of periventricular white matter disease and race. Stroke 40:530–536. doi:10.1161/STROKEAHA.108.521906
32. Kobayashi K et al (2013) Minocycline selectively inhibits M1 polarization of microglia. Cell Death Dis 4:e525. doi:10.1038/cddis.2013.54
33. Kwon MJ et al (2013) Contribution of macrophages to enhanced regenerative capacity of dorsal root ganglia sensory neurons by conditioning injury. J Neurosci 33:15095–15108. doi:10.1523/JNEUROSCI.0278-13.2013
34. Ladecola C, Anrather J (2011) The immunology of stroke: from mechanisms to translation. Nat Med 17:796–808. doi:10.1038/nm.2399
35. Lalancette-Hebert M, Gowing G, Simard A, Weng YC, Kriz J (2007) Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 27:2596–2605. doi:10.1523/JNEUROSCI.5360-06.2007
36. Lalancette-Hebert M et al (2012) Galectin-3 is required for resident microglia activation and proliferation in response to ischemic injury. J Neurosci 32:10383–10395. doi:10.1523/JNEUROSCI.1498-12.2012
37. Lehrmann E et al (1998) Microglia and macrophages are major sources of locally produced transforming growth factor-beta1 after transient middle cerebral artery occlusion in rats. Glia 24:437–448
38. Lenz KM, McCarthy MM (2015) A starring role for microglia in brain sex differences. Neuroscientist 21:306–321. doi:10.1177/1073858414536468
39. Liu Z et al (2007) Chronic treatment with minocycline preserves adult new neurons and reduces functional impairment after focal cerebral ischemia. Stroke 38:146–152. doi:10.1161/01.STR.0000251791.64910.cd
40. Loram LC et al (2012) Sex and estradiol influence glial pro-inflammatory responses to lipopolysaccharide in rats. Psychoneuroendocrinology 37:1688–1699. doi:10.1016/j.psyneuen.2012.02.018
41. Lund FE (2008) Cytokine-producing B lymphocytes-key regulators of immunity. Curr Opin Immunol 20:332–338. doi:10.1016/j.coi.2008.03.003
42. Madan R et al (2009) Nonredundant roles for B cell-derived IL-10 in immune counter-regulation. J Immunol 183:2312–2320. doi:10.4049/jimmunol.0900185
43. Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM (2000) M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 164:6166–6173
44. Miron VE et al (2013) M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat Neurosci 16:1211–1218. doi:10.1038/nn.3469
45. Moussaud S, Draheim HJ (2010) A new method to isolate microglia from adult mice and culture them for an extended period of time. J Neurosci Methods 187:243–253. doi:10.1016/j.jneumeth.2010.01.017
46. Murphy SJ, McCullough LD, Smith JM (2004) Stroke in the female: role of biological sex and estrogen. ILAR J 45:147–159
47. Onwuekwe I, Ezeala-Adikaibe B (2012) Ischemic stroke and neuroprotection. Ann Med Health Sci Res 2:186–190. doi:10.4103/2141-9248.105669
48. Owens T, Wekerle H, Antel J (2001) Genetic models for CNS inflammation. Nat Med 7:161–166. doi:10.1038/84603
49. Parada E et al (2013) The microglial alpha7-acetylcholine nicotinic receptor is a key element in promoting neuroprotection by inducing heme oxygenase-1 via nuclear factor erythroid-2-related factor 2. Antioxid Redox Signal 19:1135–1148. doi:10.1089/ars.2012.4671
50. Patel AR, Ritzel R, McCullough LD, Liu F (2013) Microglia and ischemic stroke: a double-edged sword. Int J Physiol Pathophysiol Pharmacol 5:73–90
51. Pepe G, Calderazzi G, De Maglie M, Villa A, Vegeto E (2014) Heterogeneous induction of microglia M2a phenotype by central administration of interleukin-4. J Neuroinflammation 11:1031. doi:10.1186/s12974-014-0211-6
52. Perego C, Fumagalli S, De Simoni MG (2011) Temporal pattern of expression and colocalization of microglia/macrophage phenotype markers following brain ischemic injury in mice. J Neuroinflammation 8:174. doi:10.1186/1742-2094-8-174
53. Perez-de Puig I, Miro F, Salas-Perdomo A, Bonfill-Teixidor E, Ferrer-Ferrer M, Marquez-Kisinousky L, Planas AM (2013) IL-10 deficiency exacerbates the brain inflammatory response to permanent ischemia without preventing resolution of the lesion. J Cereb Blood Flow Metab 33:1955–1966. doi:10.1038/jcbfm.2013.155
54. Pousset F, Cremona S, Dantzer R, Kelley K, Parnet P (1999) Interleukin-4 and interleukin-10 regulate IL1-beta induced mouse primary astrocyte activation: a comparative study. Glia 26:12–21
55. Ransohoff RM, Brown MA (2012) Innate immunity in the central nervous system. J Clin Invest 122:1164–1171. doi:10.1172/JCI58644
56. Rosenzweig S, Carmichael ST (2013) Age-dependent exacerbation of white matter stroke outcomes: a role for oxidative damage and inflammatory mediators. Stroke 44:2579–2586. doi:10.1161/STROKEAHA.113.001796
57. Schilling M, Besselmann M, Muller M, Strecker JK, Ringelstein EB, Kiefer R (2005) Predominant phagocytic activity of resident microglia over hematogenous macrophages following transient focal cerebral ischemia: an investigation using green fluorescent protein transgenic bone marrow chimeric mice. Exp Neurol 196:290–297. doi:10.1016/j.expneurol.2005.08.004
58. Sica A, Mantovani A (2012) Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122:787–795. doi:10.1172/JCI59643
59. Sierra A, Gottfried-Blackmore AC, McEwen BS, Bulloch K (2007) Microglia derived from aging mice exhibit an altered inflammatory profile. Glia 55:412–424. doi:10.1002/glia.20468
60. Sozmen EG, Kolekar A, Havton LA, Carmichael ST (2009) A white matter stroke model in the mouse: axonal damage, progenitor responses and MRI correlates. J Neurosci Methods 180:261–272. doi:10.1016/j.jneumeth.2009.03.017
61. Stein M, Keshav S, Harris N, Gordon S (1992) Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med 176:287–292
62. Sudlow CL, Warlow CP (1997) Comparable studies of the incidence of stroke and its pathological types: results from an international collaboration. Int Stroke Incidence Collab Stroke 28:491–499
63. Taylor RA, Sansing LH (2013) Microglial responses after ischemic stroke and intracerebral hemorrhage. Clin Dev Immunol 2013:746068. doi:10.1155/2013/746068
64. Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, Gordon S (2005) Macrophage receptors and immune recognition. Annu Rev Immunol 23:901–944. doi:10.1146/annurev.immunol.23.021704.115816
65. Thored P et al (2009) Long-term accumulation of microglia with proneurogenic phenotype concomitant with persistent neurogenesis in adult subventricular zone after stroke. Glia 57:835–849. doi:10.1002/glia.20810
66. Towfighi A, Saver JL (2011) Stroke declines from third to fourth leading cause of death in the United States: historical perspective and challenges ahead. Stroke 42:2351–2355. doi:10.1161/STROKEAHA.111.621904
67. Wang G et al (2013) Microglia/macrophage polarization dynamics in white matter after traumatic brain injury. J Cereb Blood Flow Metab 33:1864–1874. doi:10.1038/jcbfm.2013.146
68. Xiong X, Barreto GE, Xu L, Ouyang YB, Xie X, Giffard RG (2011) Increased brain injury and worsened neurological outcome in interleukin-4 knockout mice after transient focal cerebral ischemia. Stroke 42:2026–2032. doi:10.1161/STROKEAHA.110.593772
69. Zaremba J, Losy J (2001) Early TNF-alpha levels correlate with ischaemic stroke severity. Acta Neurol Scand 104:288–295
70. Zhao W, Xie W, Xiao Q, Beers DR, Appel SH (2006) Protective effects of an anti-inflammatory cytokine, interleukin-4, on motoneuron toxicity induced by activated microglia. J Neurochem 99:1176–1187. doi:10.1111/j.1471-4159.2006.04172.x