The changing phenotype of microglia from homeostasis to disease (original) (raw)

• Farber K, Kettenmann H: Purinergic signaling and microglia. Pflugers Arch 2006, 452: 615-621. 10.1007/s00424-006-0064-7
  Article PubMed CAS Google Scholar
• Hanisch UK, Kettenmann H: Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 2007, 10: 1387-1394. 10.1038/nn1997
  Article CAS PubMed Google Scholar
• Kettenmann H, Hanisch UK, Noda M, Verkhratsky A: Physiology of microglia. Physiol Rev 2011, 91: 461-553. 10.1152/physrev.00011.2010
  Article CAS PubMed Google Scholar
• Kettenmann H, Banati R, Walz W: Electrophysiological behavior of microglia. Glia 1993, 7: 93-101. 10.1002/glia.440070115
  Article CAS PubMed Google Scholar
• Noda M, Kettenmann H, Wada K: Anti-inflammatory effects of kinins via microglia in the central nervous system. Biol Chem 2006, 387: 167-171.
  Article CAS PubMed Google Scholar
• Pocock JM, Kettenmann H: Neurotransmitter receptors on microglia. Trends Neurosci 2007, 30: 527-535. 10.1016/j.tins.2007.07.007
  Article CAS PubMed Google Scholar
• Skoff RP: The fine structure of pulse labeled (3-H-thymidine cells) in degenerating rat optic nerve. J Comp Neurol 1975, 161: 595-611. 10.1002/cne.901610408
  Article CAS PubMed Google Scholar
• Kitamura T, Miyake T, Fujita S: Genesis of resting microglia in the gray matter of mouse hippocampus. J Comp Neurol 1984, 226: 421-433. 10.1002/cne.902260310
  Article CAS PubMed Google Scholar
• Alliot F, Lecain E, Grima B, Pessac B: Microglial progenitors with a high proliferative potential in the embryonic and adult mouse brain. Proc Natl Acad Sci U S A 1991, 88: 1541-1545. 10.1073/pnas.88.4.1541
  Article PubMed Central CAS PubMed Google Scholar
• Priller J, Flugel A, Wehner T, Boentert M, Haas CA, Prinz M, Fernandez-Klett F, Prass K, Bechmann I, de Boer BA, et al.: Targeting gene-modified hematopoietic cells to the central nervous system: use of green fluorescent protein uncovers microglial engraftment. Nat Med 2001, 7: 1356-1361. 10.1038/nm1201-1356
  Article CAS PubMed Google Scholar
• Ritter MR, Banin E, Moreno SK, Aguilar E, Dorrell MI, Friedlander M: Myeloid progenitors differentiate into microglia and promote vascular repair in a model of ischemic retinopathy. J Clin Invest 2006, 116: 3266-3276. 10.1172/JCI29683
  Article PubMed Central CAS PubMed Google Scholar
• Ling EA, Penney D, Leblond CP: Use of carbon labeling to demonstrate the role of blood monocytes as precursors of the 'ameboid cells’ present in the corpus callosum of postnatal rats. J Comp Neurol 1980, 193: 631-657. 10.1002/cne.901930304
  Article CAS PubMed Google Scholar
• Davoust N, Vuaillat C, Cavillon G, Domenget C, Hatterer E, Bernard A, Dumontel C, Jurdic P, Malcus C, Confavreux C, et al.: Bone marrow CD34+/B220+ progenitors target the inflamed brain and display in vitro differentiation potential toward microglia. Faseb J 2006, 20: 2081-2092. 10.1096/fj.05-5593com
  Article CAS PubMed Google Scholar
• Schmitz G, Leuthauser-Jaschinski K, Orso E: Are circulating monocytes as microglia orthologues appropriate biomarker targets for neuronal diseases? Cent Nerv Syst Agents Med Chem 2009, 9: 307-330.
  Article CAS PubMed Google Scholar
• Djukic M, Mildner A, Schmidt H, Czesnik D, Bruck W, Priller J, Nau R, Prinz M: Circulating monocytes engraft in the brain, differentiate into microglia and contribute to the pathology following meningitis in mice. Brain 2006, 129: 2394-2403. 10.1093/brain/awl206
  Article PubMed Google Scholar
• Templeton SP, Kim TS, O’Malley K, Perlman S: Maturation and localization of macrophages and microglia during infection with a neurotropic murine coronavirus. Brain Pathol 2008, 18: 40-51. 10.1111/j.1750-3639.2007.00098.x
  Article PubMed Google Scholar
• Liu M, Eguchi N, Yamasaki Y, Urade Y, Hattori N, Urabe T: Focal cerebral ischemia/reperfusion injury in mice induces hematopoietic prostaglandin D synthase in microglia and macrophages. Neuroscience 2007, 145: 520-529. 10.1016/j.neuroscience.2006.12.018
  Article CAS PubMed Google Scholar
• Luo X, Carlson KA, Wojna V, Mayo R, Biskup TM, Stoner J, Anderson J, Gendelman HE, Melendez LM: Macrophage proteomic fingerprinting predicts HIV-1-associated cognitive impairment. Neurology 2003, 60: 1931-1937. 10.1212/01.WNL.0000064396.54554.26
  Article CAS PubMed Google Scholar
• Balasubramaniam B, Carter DA, Mayer EJ, Dick AD: Microglia derived IL-6 suppresses neurosphere generation from adult human retinal cell suspensions. Exp Eye Res 2009, 89: 757-766. 10.1016/j.exer.2009.06.019
  Article CAS PubMed Google Scholar
• Dheen ST, Jun Y, Yan Z, Tay SS, Ling EA: Retinoic acid inhibits expression of TNF-alpha and iNOS in activated rat microglia. Glia 2005, 50: 21-31. 10.1002/glia.20153
  Article PubMed Google Scholar
• Bi XL, Yang JY, Dong YX, Wang JM, Cui YH, Ikeshima T, Zhao YQ, Wu CF: Resveratrol inhibits nitric oxide and TNF-alpha production by lipopolysaccharide-activated microglia. Int Immunopharmacol 2005, 5: 185-193. 10.1016/j.intimp.2004.08.008
  Article CAS PubMed Google Scholar
• Moss DW, Bates TE: Activation of murine microglial cell lines by lipopolysaccharide and interferon-gamma causes NO-mediated decreases in mitochondrial and cellular function. Eur J Neurosci 2001, 13: 529-538. 10.1046/j.1460-9568.2001.01418.x
  Article CAS PubMed Google Scholar
• Liu B, Gao HM, Wang JY, Jeohn GH, Cooper CL, Hong JS: Role of nitric oxide in inflammation-mediated neurodegeneration. Ann N Y Acad Sci 2002, 962: 318-331. 10.1111/j.1749-6632.2002.tb04077.x
  Article CAS PubMed Google Scholar
• Colton CA, Gilbert DL: Production of superoxide anions by a CNS macrophage, the microglia. FEBS Lett 1987, 223: 284-288. 10.1016/0014-5793(87)80305-8
  Article CAS PubMed Google Scholar
• Mao H, Liu B: Synergistic microglial reactive oxygen species generation induced by pesticides lindane and dieldrin. Neuroreport 2008, 19: 1317-1320. 10.1097/WNR.0b013e32830b3677
  Article CAS PubMed Google Scholar
• Cagnin A, Brooks DJ, Kennedy AM, Gunn RN, Myers R, Turkheimer FE, Jones T, Banati RB: In-vivo measurement of activated microglia in dementia. Lancet 2001, 358: 461-467. 10.1016/S0140-6736(01)05625-2
  Article CAS PubMed Google Scholar
• McGeer PL, Itagaki S, Tago H, McGeer EG: Reactive microglia in patients with senile dementia of the Alzheimer type are positive for the histocompatibility glycoprotein HLA-DR. Neurosci Lett 1987, 79: 195-200. 10.1016/0304-3940(87)90696-3
  Article CAS PubMed Google Scholar
• Imamura K, Hishikawa N, Sawada M, Nagatsu T, Yoshida M, Hashizume Y: Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson’s disease brains. Acta Neuropathol 2003, 106: 518-526. 10.1007/s00401-003-0766-2
  Article CAS PubMed Google Scholar
• Lawson LJ, Perry VH, Dri P, Gordon S: Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 1990, 39: 151-170. 10.1016/0306-4522(90)90229-W
  Article CAS PubMed Google Scholar
• Loeffler DA, DeMaggio AJ, Juneau PL, Havaich MK, LeWitt PA: Effects of enhanced striatal dopamine turnover in vivo on glutathione oxidation. Clin Neuropharmacol 1994, 17: 370-379. 10.1097/00002826-199408000-00009
  Article CAS PubMed Google Scholar
• Castano A, Herrera AJ, Cano J, Machado A: Lipopolysaccharide intranigral injection induces inflammatory reaction and damage in nigrostriatal dopaminergic system. J Neurochem 1998, 70: 1584-1592.
  Article CAS PubMed Google Scholar
• Liu B, Jiang JW, Wilson BC, Du L, Yang SN, Wang JY, Wu GC, Cao XD, Hong JS: Systemic infusion of naloxone reduces degeneration of rat substantia nigral dopaminergic neurons induced by intranigral injection of lipopolysaccharide. J Pharmacol Exp Ther 2000, 295: 125-132.
  CAS PubMed Google Scholar
• Lu X, Bing G, Hagg T: Naloxone prevents microglia-induced degeneration of dopaminergic substantia nigra neurons in adult rats. Neuroscience 2000, 97: 285-291. 10.1016/S0306-4522(00)00033-6
  Article CAS PubMed Google Scholar
• Cartier L, Hartley O, Dubois-Dauphin M, Krause KH: Chemokine receptors in the central nervous system: role in brain inflammation and neurodegenerative diseases. Brain Res Brain Res Rev 2005, 48: 16-42.
  Article CAS PubMed Google Scholar
• Duan Y, Sahley CL, Muller KJ: ATP and NO dually control migration of microglia to nerve lesions. Dev Neurobiol 2009, 69: 60-72. 10.1002/dneu.20689
  Article PubMed Central CAS PubMed Google Scholar
• Farinas I, Cano-Jaimez M, Bellmunt E, Soriano M: Regulation of neurogenesis by neurotrophins in developing spinal sensory ganglia. Brain Res Bull 2002, 57: 809-816. 10.1016/S0361-9230(01)00767-5
  Article CAS PubMed Google Scholar
• Markus A, Patel TD, Snider WD: Neurotrophic factors and axonal growth. Curr Opin Neurobiol 2002, 12: 523-531. 10.1016/S0959-4388(02)00372-0
  Article CAS PubMed Google Scholar
• Oppenheim RW, Prevette D, Tytell M, Homma S: Naturally occurring and induced neuronal death in the chick embryo in vivo requires protein and RNA synthesis: evidence for the role of cell death genes. Dev Biol 1990, 138: 104-113. 10.1016/0012-1606(90)90180-Q
  Article CAS PubMed Google Scholar
• Miller FD, Kaplan DR: Neurotrophin signalling pathways regulating neuronal apoptosis. Cell Mol Life Sci 2001, 58: 1045-1053. 10.1007/PL00000919
  Article CAS PubMed Google Scholar
• Nimmerjahn A, Kirchhoff F, Helmchen F: Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308: 1314-1318. 10.1126/science.1110647
  Article CAS PubMed Google Scholar
• Battisti WP, Wang J, Bozek K, Murray M: Macrophages, microglia, and astrocytes are rapidly activated after crush injury of the goldfish optic nerve: a light and electron microscopic analysis. J Comp Neurol 1995, 354: 306-320. 10.1002/cne.903540211
  Article CAS PubMed Google Scholar
• Hao HP, Doh-Ura K, Nakanishi H: Impairment of microglial responses to facial nerve axotomy in cathepsin S-deficient mice. J Neurosci Res 2007, 85: 2196-2206. 10.1002/jnr.21357
  Article CAS PubMed Google Scholar
• Sawada H, Hishida R, Hirata Y, Ono K, Suzuki H, Muramatsu S, Nakano I, Nagatsu T, Sawada M: Activated microglia affect the nigro-striatal dopamine neurons differently in neonatal and aged mice treated with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. J Neurosci Res 2007, 85: 1752-1761. 10.1002/jnr.21241
  Article CAS PubMed Google Scholar
• Shaked I, Tchoresh D, Gersner R, Meiri G, Mordechai S, Xiao X, Hart RP, Schwartz M: Protective autoimmunity: interferon-gamma enables microglia to remove glutamate without evoking inflammatory mediators. J Neurochem 2005, 92: 997-1009. 10.1111/j.1471-4159.2004.02954.x
  Article CAS PubMed Google Scholar
• Bruccoleri A, Harry GJ: Chemical-induced hippocampal neurodegeneration and elevations in TNFalpha, TNFbeta, IL-1alpha, IP-10, and MCP-1 mRNA in osteopetrotic (op/op) mice. J Neurosci Res 2000, 62: 146-155. 10.1002/1097-4547(20001001)62:1<146::AID-JNR15>3.0.CO;2-L
  Article CAS PubMed Google Scholar
• Lalancette-Hebert M, Gowing G, Simard A, Weng YC, Kriz J: Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 2007, 27: 2596-2605. 10.1523/JNEUROSCI.5360-06.2007
  Article CAS PubMed Google Scholar
• Lambertsen KL, Clausen BH, Babcock AA, Gregersen R, Fenger C, Nielsen HH, Haugaard LS, Wirenfeldt M, Nielsen M, Dagnaes-Hansen F, et al.: Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neurosci 2009, 29: 1319-1330. 10.1523/JNEUROSCI.5505-08.2009
  Article CAS PubMed Google Scholar
• Napoli I, Neumann H: Protective effects of microglia in multiple sclerosis. Exp Neurol 2010, 225: 24-28. 10.1016/j.expneurol.2009.04.024
  Article PubMed Google Scholar
• Rapalino O, Lazarov-Spiegler O, Agranov E, Velan GJ, Yoles E, Fraidakis M, Solomon A, Gepstein R, Katz A, Belkin M, et al.: Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat Med 1998, 4: 814-821. 10.1038/nm0798-814
  Article CAS PubMed Google Scholar
• Rabchevsky AG, Streit WJ: Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth. J Neurosci Res 1997, 47: 34-48. 10.1002/(SICI)1097-4547(19970101)47:1<34::AID-JNR4>3.0.CO;2-G
  Article CAS PubMed Google Scholar
• Morigiwa K, Quan M, Murakami M, Yamashita M, Fukuda Y: P2 Purinoceptor expression and functional changes of hypoxia-activated cultured rat retinal microglia. Neurosci Lett 2000, 282: 153-156. 10.1016/S0304-3940(00)00887-9
  Article CAS PubMed Google Scholar
• Bosco A, Steele MR, Vetter ML: Early microglia activation in a mouse model of chronic glaucoma. J Comp Neurol 2011, 519: 599-620. 10.1002/cne.22516
  Article PubMed Central PubMed Google Scholar
• Hur J, Lee P, Kim MJ, Kim Y, Cho YW: Ischemia-activated microglia induces neuronal injury via activation of gp91phox NADPH oxidase. Biochem Biophys Res Commun 2010, 391: 1526-1530. 10.1016/j.bbrc.2009.12.114
  Article CAS PubMed Google Scholar
• Maeda M, Tsuda M, Tozaki-Saitoh H, Inoue K, Kiyama H: Nerve injury-activated microglia engulf myelinated axons in a P2Y12 signaling-dependent manner in the dorsal horn. Glia 2010, 58: 1838-1846. 10.1002/glia.21053
  Article PubMed Google Scholar
• Lee EJ, Woo MS, Moon PG, Baek MC, Choi IY, Kim WK, Junn E, Kim HS: Alpha-synuclein activates microglia by inducing the expressions of matrix metalloproteinases and the subsequent activation of protease-activated receptor-1. J Immunol 2010, 185: 615-623. 10.4049/jimmunol.0903480
  Article CAS PubMed Google Scholar
• Su X, Maguire-Zeiss KA, Giuliano R, Prifti L, Venkatesh K, Federoff HJ: Synuclein activates microglia in a model of Parkinson’s disease. Neurobiol Aging 2008, 29: 1690-1701. 10.1016/j.neurobiolaging.2007.04.006
  Article PubMed Central CAS PubMed Google Scholar
• Zhang W, Wang T, Pei Z, Miller DS, Wu X, Block ML, Wilson B, Zhang W, Zhou Y, Hong JS, Zhang J: Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson’s disease. Faseb J 2005, 19: 533-542. 10.1096/fj.04-2751com
  Article CAS PubMed Google Scholar
• Jana M, Palencia CA, Pahan K: Fibrillar amyloid-beta peptides activate microglia via TLR2: implications for Alzheimer’s disease. J Immunol 2008, 181: 7254-7262.
  Article PubMed Central CAS PubMed Google Scholar
• Piers TM, Heales SJ, Pocock JM: Positive allosteric modulation of metabotropic glutamate receptor 5 down-regulates fibrinogen-activated microglia providing neuronal protection. Neurosci Lett 2011, 505: 140-145. 10.1016/j.neulet.2011.10.007
  Article CAS PubMed Google Scholar
• Lee DY, Oh YJ, Jin BK: Thrombin-activated microglia contribute to death of dopaminergic neurons in rat mesencephalic cultures: dual roles of mitogen-activated protein kinase signaling pathways. Glia 2005, 51: 98-110. 10.1002/glia.20190
  Article PubMed Google Scholar
• Siao CJ, Tsirka SE: Tissue plasminogen activator mediates microglial activation via its finger domain through annexin II. J Neurosci 2002, 22: 3352-3358.
  CAS PubMed Google Scholar
• Milner R, Crocker SJ, Hung S, Wang X, Frausto RF, del Zoppo GJ: Fibronectin- and vitronectin-induced microglial activation and matrix metalloproteinase-9 expression is mediated by integrins alpha5beta1 and alphavbeta5. J Immunol 2007, 178: 8158-8167.
  Article CAS PubMed Google Scholar
• Kim YS, Kim SS, Cho JJ, Choi DH, Hwang O, Shin DH, Chun HS, Beal MF, Joh TH: Matrix metalloproteinase-3: a novel signaling proteinase from apoptotic neuronal cells that activates microglia. J Neurosci 2005, 25: 3701-3711. 10.1523/JNEUROSCI.4346-04.2005
  Article CAS PubMed Google Scholar
• del Zoppo GJ, Milner R, Mabuchi T, Hung S, Wang X, Berg GI, Koziol JA: Microglial activation and matrix protease generation during focal cerebral ischemia. Stroke 2007, 38: 646-651. 10.1161/01.STR.0000254477.34231.cb
  Article CAS PubMed Google Scholar
• Matsui T, Motoki Y, Inomoto T, Miura D, Kato Y, Suenaga H, Hino K, Nojima J: Temperature-Related Effects of Adenosine Triphosphate-Activated Microglia on Pro-Inflammatory Factors. Neurocrit Care 2011.
  Google Scholar
• Yasuda Y, Shimoda T, Uno K, Tateishi N, Furuya S, Yagi K, Suzuki K, Fujita S: The effects of MPTP on the activation of microglia/astrocytes and cytokine/chemokine levels in different mice strains. J Neuroimmunol 2008, 204: 43-51. 10.1016/j.jneuroim.2008.08.003
  Article CAS PubMed Google Scholar
• Gao HM, Hong JS, Zhang W, Liu B: Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons. J Neurosci 2002, 22: 782-790.
  CAS PubMed Google Scholar
• Wu XF, Block ML, Zhang W, Qin L, Wilson B, Zhang WQ, Veronesi B, Hong JS: The role of microglia in paraquat-induced dopaminergic neurotoxicity. Antioxid Redox Signal 2005, 7: 654-661. 10.1089/ars.2005.7.654
  Article CAS PubMed Google Scholar
• McClain JA, Morris SA, Deeny MA, Marshall SA, Hayes DM, Kiser ZM, Nixon K: Adolescent binge alcohol exposure induces long-lasting partial activation of microglia. Brain Behav Immun 2011, 25(Suppl 1):S120-S128.
  Article PubMed Central CAS PubMed Google Scholar
• Kuhn DM, Francescutti-Verbeem DM, Thomas DM: Dopamine quinones activate microglia and induce a neurotoxic gene expression profile: relationship to methamphetamine-induced nerve ending damage. Ann N Y Acad Sci 2006, 1074: 31-41. 10.1196/annals.1369.003
  Article CAS PubMed Google Scholar
• Lu DY, Tang CH, Chen YH, Wei IH: Berberine suppresses neuroinflammatory responses through AMP-activated protein kinase activation in BV-2 microglia. J Cell Biochem 2010, 110: 697-705. 10.1002/jcb.22580
  Article CAS PubMed Google Scholar
• Jung HW, Oh TW, Jung JK, Lee JH, Shin GJ, Park YK: Inhibitory Effects of the Methylene Chloride Fraction of JP05 on the Production of Inflammatory Mediators in LPS-activated BV2 Microglia. Inflammation 2010, 35: 332-341.
  Article CAS Google Scholar
• Meng XL, Yang JY, Chen GL, Zhang LJ, Wang LH, Li J, Wang JM, Wu CF: RV09, a novel resveratrol analogue, inhibits NO and TNF-alpha production by LPS-activated microglia. Int Immunopharmacol 2008, 8: 1074-1082. 10.1016/j.intimp.2008.03.011
  Article CAS PubMed Google Scholar
• Xu Y, Xue Y, Wang Y, Feng D, Lin S, Xu L: Multiple-modulation effects of Oridonin on the production of proinflammatory cytokines and neurotrophic factors in LPS-activated microglia. Int Immunopharmacol 2009, 9: 360-365. 10.1016/j.intimp.2009.01.002
  Article CAS PubMed Google Scholar
• Iribarren P, Chen K, Hu J, Zhang X, Gong W, Wang JM: IL-4 inhibits the expression of mouse formyl peptide receptor 2, a receptor for amyloid beta1-42, in TNF-alpha-activated microglia. J Immunol 2005, 175: 6100-6106.
  Article CAS PubMed Google Scholar
• Krady JK, Lin HW, Liberto CM, Basu A, Kremlev SG, Levison SW: Ciliary neurotrophic factor and interleukin-6 differentially activate microglia. J Neurosci Res 2008, 86: 1538-1547. 10.1002/jnr.21620
  Article CAS PubMed Google Scholar
• Tamakawa N, Saio M, Suwa T, Ohe N, Yoshimura S, Iwama T, Shinoda J, Sakai N, Takami T: Interleukin-2 activated microglia engulf tumor infiltrating T cells in the central nervous system. Int J Mol Med 2004, 13: 497-503.
  CAS PubMed Google Scholar
• Natarajan C, Sriram S, Muthian G, Bright JJ: Signaling through JAK2-STAT5 pathway is essential for IL-3-induced activation of microglia. Glia 2004, 45: 188-196. 10.1002/glia.10316
  Article PubMed Google Scholar
• Rozenfeld C, Martinez R, Seabra S, Sant’anna C, Goncalves JG, Bozza M, Moura-Neto V, De Souza W: Toxoplasma gondii prevents neuron degeneration by interferon-gamma-activated microglia in a mechanism involving inhibition of inducible nitric oxide synthase and transforming growth factor-beta1 production by infected microglia. Am J Pathol 2005, 167: 1021-1031. 10.1016/S0002-9440(10)61191-1
  Article PubMed Central CAS PubMed Google Scholar
• Hall GL, Girdlestone J, Compston DA, Wing MG: Recall antigen presentation by gamma-interferon-activated microglia results in T cell activation and propagation of the immune response. J Neuroimmunol 1999, 98: 105-111. 10.1016/S0165-5728(99)00069-7
  Article CAS PubMed Google Scholar
• Kim KS, Park JY, Jou I, Park SM: Functional implication of BAFF synthesis and release in gangliosides-stimulated microglia. J Leukoc Biol 2009, 86: 349-359. 10.1189/jlb.1008659
  Article CAS PubMed Google Scholar
• Min KJ, Yang MS, Kim SU, Jou I, Joe EH: Astrocytes induce hemeoxygenase-1 expression in microglia: a feasible mechanism for preventing excessive brain inflammation. J Neurosci 2006, 26: 1880-1887. 10.1523/JNEUROSCI.3696-05.2006
  Article CAS PubMed Google Scholar
• Zheng H, Zhu W, Zhao H, Wang X, Wang W, Li Z: Kainic acid-activated microglia mediate increased excitability of rat hippocampal neurons in vitro and in vivo: crucial role of interleukin-1beta. Neuroimmunomodulation 2010, 17: 31-38. 10.1159/000243083
  Article CAS PubMed Google Scholar
• Zhu W, Zheng H, Shao X, Wang W, Yao Q, Li Z: Excitotoxicity of TNFalpha derived from KA activated microglia on hippocampal neurons in vitro and in vivo. J Neurochem 2010, 114: 386-396. 10.1111/j.1471-4159.2010.06763.x
  Article CAS PubMed Google Scholar
• Aloisi F: Immune function of microglia. Glia 2001, 36: 165-179. 10.1002/glia.1106
  Article CAS PubMed Google Scholar
• Neumann J, Sauerzweig S, Ronicke R, Gunzer F, Dinkel K, Ullrich O, Gunzer M, Reymann KG: Microglia cells protect neurons by direct engulfment of invading neutrophil granulocytes: a new mechanism of CNS immune privilege. J Neurosci 2008, 28: 5965-5975. 10.1523/JNEUROSCI.0060-08.2008
  Article CAS PubMed Google Scholar
• Lee CY, Landreth GE: The role of microglia in amyloid clearance from the AD brain. J Neural Transm 2010, 117: 949-960. 10.1007/s00702-010-0433-4
  Article CAS PubMed Google Scholar
• Teismann P, Schulz JB: Cellular pathology of Parkinson’s disease: astrocytes, microglia and inflammation. Cell Tissue Res 2004, 318: 149-161. 10.1007/s00441-004-0944-0
  Article PubMed Google Scholar
• Hill KE, Zollinger LV, Watt HE, Carlson NG, Rose JW: Inducible nitric oxide synthase in chronic active multiple sclerosis plaques: distribution, cellular expression and association with myelin damage. J Neuroimmunol 2004, 151: 171-179. 10.1016/j.jneuroim.2004.02.005
  Article CAS PubMed Google Scholar
• Mandrekar-Colucci S, Landreth GE: Microglia and inflammation in Alzheimer’s disease. CNS Neurol Disord Drug Targets 2010, 9: 156-167.
  Article CAS PubMed Google Scholar
• Kreutzberg GW: Microglia: a sensor for pathological events in the CNS. Trends Neurosci 1996, 19: 312-318. 10.1016/0166-2236(96)10049-7
  Article CAS PubMed Google Scholar
• Schwartz M, Butovsky O, Bruck W, Hanisch UK: Microglial phenotype: is the commitment reversible? Trends Neurosci 2006, 29: 68-74. 10.1016/j.tins.2005.12.005
  Article CAS PubMed Google Scholar
• Hanisch UK: Microglia as a source and target of cytokines. Glia 2002, 40: 140-155. 10.1002/glia.10161
  Article PubMed Google Scholar
• Biber K, Neumann H, Inoue K, Boddeke HW: Neuronal ‘On’ and ‘Off’ signals control microglia. Trends Neurosci 2007, 30: 596-602. 10.1016/j.tins.2007.08.007
  Article CAS PubMed Google Scholar
• Polazzi E, Contestabile A: Reciprocal interactions between microglia and neurons: from survival to neuropathology. Rev Neurosci 2002, 13: 221-242.
  PubMed Google Scholar
• Zhou Y, Wang Y, Kovacs M, Jin J, Zhang J: Microglial activation induced by neurodegeneration: a proteomic analysis. Mol Cell Proteomics 2005, 4: 1471-1479. 10.1074/mcp.M500114-MCP200
  Article CAS PubMed Google Scholar
• Hoek RM, Ruuls SR, Murphy CA, Wright GJ, Goddard R, Zurawski SM, Blom B, Homola ME, Streit WJ, Brown MH, et al.: Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science 2000, 290: 1768-1771.
  Article CAS PubMed Google Scholar
• Chitnis T, Imitola J, Wang Y, Elyaman W, Chawla P, Sharuk M, Raddassi K, Bronson RT, Khoury SJ: Elevated neuronal expression of CD200 protects Wlds mice from inflammation-mediated neurodegeneration. Am J Pathol 2007, 170: 1695-1712. 10.2353/ajpath.2007.060677
  Article PubMed Central CAS PubMed Google Scholar
• Neumann H: Control of glial immune function by neurons. Glia 2001, 36: 191-199. 10.1002/glia.1108
  Article CAS PubMed Google Scholar
• Wei R, Jonakait GM: Neurotrophins and the anti-inflammatory agents interleukin-4 (IL-4), IL-10, IL-11 and transforming growth factor-beta1 (TGF-beta1) down-regulate T cell costimulatory molecules B7 and CD40 on cultured rat microglia. J Neuroimmunol 1999, 95: 8-18. 10.1016/S0165-5728(98)00248-3
  Article CAS PubMed Google Scholar
• Fukui K, Urano S, Koike T: Releasing factors from mature neurons modulate microglial survival via purinergic receptor activation. Neurosci Lett 2009, 456: 64-68. 10.1016/j.neulet.2009.03.092
  Article CAS PubMed Google Scholar
• Gehrmann J, Banati RB: Microglial turnover in the injured CNS: activated microglia undergo delayed DNA fragmentation following peripheral nerve injury. J Neuropathol Exp Neurol 1995, 54: 680-688. 10.1097/00005072-199509000-00010
  Article CAS PubMed Google Scholar
• Kuhlmann T, Bitsch A, Stadelmann C, Siebert H, Bruck W: Macrophages are eliminated from the injured peripheral nerve via local apoptosis and circulation to regional lymph nodes and the spleen. J Neurosci 2001, 21: 3401-3408.
  CAS PubMed Google Scholar
• Shuman SL, Bresnahan JC, Beattie MS: Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J Neurosci Res 1997, 50: 798-808. 10.1002/(SICI)1097-4547(19971201)50:5<798::AID-JNR16>3.0.CO;2-Y
  Article CAS PubMed Google Scholar
• White CA, McCombe PA, Pender MP: Microglia are more susceptible than macrophages to apoptosis in the central nervous system in experimental autoimmune encephalomyelitis through a mechanism not involving Fas (CD95). Int Immunol 1998, 10: 935-941. 10.1093/intimm/10.7.935
  Article CAS PubMed Google Scholar
• Pais TF, Figueiredo C, Peixoto R, Braz MH, Chatterjee S: Necrotic neurons enhance microglial neurotoxicity through induction of glutaminase by a MyD88-dependent pathway. J Neuroinflammation 2008, 5: 43. 10.1186/1742-2094-5-43
  Article PubMed Central PubMed CAS Google Scholar
• Eleuteri S, Polazzi E, Contestabile A: Neuroprotection of microglia conditioned media from apoptotic death induced by staurosporine and glutamate in cultures of rat cerebellar granule cells. Neurosci Lett 2008, 448: 74-78. 10.1016/j.neulet.2008.09.033
  Article CAS PubMed Google Scholar
• Moran LB, Graeber MB: The facial nerve axotomy model. Brain Res Brain Res Rev 2004, 44: 154-178.
  Article PubMed Google Scholar
• Nakajima K, Tohyama Y, Maeda S, Kohsaka S, Kurihara T: Neuronal regulation by which microglia enhance the production of neurotrophic factors for GABAergic, catecholaminergic, and cholinergic neurons. Neurochem Int 2007, 50: 807-820. 10.1016/j.neuint.2007.02.006
  Article CAS PubMed Google Scholar
• Shih AY, Fernandes HB, Choi FY, Kozoriz MG, Liu Y, Li P, Cowan CM, Klegeris A: Policing the police: astrocytes modulate microglial activation. J Neurosci 2006, 26: 3887-3888. 10.1523/JNEUROSCI.0936-06.2006
  Article CAS PubMed Google Scholar
• Rohl C, Sievers J: Microglia is activated by astrocytes in trimethyltin intoxication. Toxicol Appl Pharmacol 2005, 204: 36-45. 10.1016/j.taap.2004.08.007
  Article PubMed CAS Google Scholar
• Ovanesov MV, Ayhan Y, Wolbert C, Moldovan K, Sauder C, Pletnikov MV: Astrocytes play a key role in activation of microglia by persistent Borna disease virus infection. J Neuroinflammation 2008, 5: 50. 10.1186/1742-2094-5-50
  Article PubMed Central PubMed CAS Google Scholar
• von Bernhardi R, Eugenin J: Microglial reactivity to beta-amyloid is modulated by astrocytes and proinflammatory factors. Brain Res 2004, 1025: 186-193. 10.1016/j.brainres.2004.07.084
  Article CAS PubMed Google Scholar
• Ramirez G, Toro R, Dobeli H, von Bernhardi R: Protection of rat primary hippocampal cultures from A beta cytotoxicity by pro-inflammatory molecules is mediated by astrocytes. Neurobiol Dis 2005, 19: 243-254. 10.1016/j.nbd.2005.01.007
  Article CAS PubMed Google Scholar
• Aloisi F, Penna G, Cerase J, Menendez Iglesias B, Adorini L: IL-12 production by central nervous system microglia is inhibited by astrocytes. J Immunol 1997, 159: 1604-1612.
  CAS PubMed Google Scholar
• Pyo H, Yang MS, Jou I, Joe EH: Wortmannin enhances lipopolysaccharide-induced inducible nitric oxide synthase expression in microglia in the presence of astrocytes in rats. Neurosci Lett 2003, 346: 141-144. 10.1016/S0304-3940(03)00505-6
  Article CAS PubMed Google Scholar
• Vincent VA, Van Dam AM, Persoons JH, Schotanus K, Steinbusch HW, Schoffelmeer AN, Berkenbosch F: Gradual inhibition of inducible nitric oxide synthase but not of interleukin-1 beta production in rat microglial cells of endotoxin-treated mixed glial cell cultures. Glia 1996, 17: 94-102. 10.1002/(SICI)1098-1136(199606)17:2<94::AID-GLIA2>3.0.CO;2-6
  Article CAS PubMed Google Scholar
• Rouach N, Calvo CF, Glowinski J, Giaume C: Brain macrophages inhibit gap junctional communication and downregulate connexin 43 expression in cultured astrocytes. Eur J Neurosci 2002, 15: 403-407. 10.1046/j.0953-816x.2001.01868.x
  Article CAS PubMed Google Scholar
• Rouach N, Calvo CF, Duquennoy H, Glowinski J, Giaume C: Hydrogen peroxide increases gap junctional communication and induces astrocyte toxicity: regulation by brain macrophages. Glia 2004, 45: 28-38. 10.1002/glia.10300
  Article PubMed Google Scholar
• Meme W, Calvo CF, Froger N, Ezan P, Amigou E, Koulakoff A, Giaume C: Proinflammatory cytokines released from microglia inhibit gap junctions in astrocytes: potentiation by beta-amyloid. Faseb J 2006, 20: 494-496.
  CAS PubMed Google Scholar
• Rohl C, Armbrust E, Kolbe K, Lucius R, Maser E, Venz S, Gulden M: Activated microglia modulate astroglial enzymes involved in oxidative and inflammatory stress and increase the resistance of astrocytes to oxidative stress in vitro. Glia 2008, 56: 1114-1126. 10.1002/glia.20683
  Article PubMed Google Scholar
• McCann MJ, O’Callaghan JP, Martin PM, Bertram T, Streit WJ: Differential activation of microglia and astrocytes following trimethyl tin-induced neurodegeneration. Neuroscience 1996, 72: 273-281. 10.1016/0306-4522(95)00526-9
  Article CAS PubMed Google Scholar
• Griffin WS: Inflammation and neurodegenerative diseases. Am J Clin Nutr 2006, 83: 470S-474S.
  CAS PubMed Google Scholar
• Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB: ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 2005, 8: 752-758. 10.1038/nn1472
  Article CAS PubMed Google Scholar
• Verderio C, Matteoli M: ATP mediates calcium signaling between astrocytes and microglial cells: modulation by IFN-gamma. J Immunol 2001, 166: 6383-6391.
  Article CAS PubMed Google Scholar
• Liu W, Tang Y, Feng J: Cross talk between activation of microglia and astrocytes in pathological conditions in the central nervous system. Life Sci 2011, 89: 141-146. 10.1016/j.lfs.2011.05.011
  Article CAS PubMed Google Scholar
• Giulian D, Baker TJ: Peptides released by ameboid microglia regulate astroglial proliferation. J Cell Biol 1985, 101: 2411-2415. 10.1083/jcb.101.6.2411
  Article CAS PubMed Google Scholar
• Tilleux S, Berger J, Hermans E: Induction of astrogliosis by activated microglia is associated with a down-regulation of metabotropic glutamate receptor 5. J Neuroimmunol 2007, 189: 23-30. 10.1016/j.jneuroim.2007.06.011
  Article CAS PubMed Google Scholar
• Savli H, Gulkac MD, Esen N: The effect of stimulated microglia conditioned media on BDNF gene expression of striatal astrocytes: quantification by real-time PCR. Int J Neurosci 2004, 114: 1601-1612. 10.1080/00207450490476138
  Article CAS PubMed Google Scholar
• Engelhardt B, Ransohoff RM: The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol 2005, 26: 485-495. 10.1016/j.it.2005.07.004
  Article CAS PubMed Google Scholar
• Re F, Belyanskaya SL, Riese RJ, Cipriani B, Fischer FR, Granucci F, Ricciardi-Castagnoli P, Brosnan C, Stern LJ, Strominger JL, Santambrogio L: Granulocyte-macrophage colony-stimulating factor induces an expression program in neonatal microglia that primes them for antigen presentation. J Immunol 2002, 169: 2264-2273.
  Article CAS PubMed Google Scholar
• Monsonego A, Imitola J, Zota V, Oida T, Weiner HL: Microglia-mediated nitric oxide cytotoxicity of T cells following amyloid beta-peptide presentation to Th1 cells. J Immunol 2003, 171: 2216-2224.
  Article CAS PubMed Google Scholar
• Shaked I, Porat Z, Gersner R, Kipnis J, Schwartz M: Early activation of microglia as antigen-presenting cells correlates with T cell-mediated protection and repair of the injured central nervous system. J Neuroimmunol 2004, 146: 84-93. 10.1016/j.jneuroim.2003.10.049
  Article CAS PubMed Google Scholar
• Goldman JE, Reynolds R: A reappraisal of ganglioside GD3 expression in the CNS. Glia 1996, 16: 291-295. 10.1002/(SICI)1098-1136(199604)16:4<291::AID-GLIA1>3.0.CO;2-3
  Article CAS PubMed Google Scholar
• Kipnis J, Avidan H, Caspi RR, Schwartz M: Dual effect of CD4 + CD25+ regulatory T cells in neurodegeneration: a dialogue with microglia. Proc Natl Acad Sci U S A 2004, 101(Suppl 2):14663-14669.
  Article PubMed Central CAS PubMed Google Scholar
• Beers DR, Henkel JS, Zhao W, Wang J, Appel SH: CD4+ T cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS. Proc Natl Acad Sci U S A 2008, 105: 15558-15563. 10.1073/pnas.0807419105
  Article PubMed Central CAS PubMed Google Scholar
• Ghasemlou N, Jeong SY, Lacroix S, David S: T cells contribute to lysophosphatidylcholine-induced macrophage activation and demyelination in the CNS. Glia 2007, 55: 294-302. 10.1002/glia.20449
  Article PubMed Google Scholar
• Levesque S, Wilson B, Gregoria V, Thorpe LB, Dallas S, Polikov VS, Hong JS, Block ML: Reactive microgliosis: extracellular micro-calpain and microglia-mediated dopaminergic neurotoxicity. Brain 2010, 133: 808-821. 10.1093/brain/awp333
  Article PubMed Central PubMed Google Scholar
• Harry GJ, Kraft AD: Neuroinflammation and microglia: considerations and approaches for neurotoxicity assessment. Expert Opin Drug Metab Toxicol 2008, 4: 1265-1277. 10.1517/17425255.4.10.1265
  Article PubMed Central CAS PubMed Google Scholar
• Knoch ME, Hartnett KA, Hara H, Kandler K, Aizenman E: Microglia induce neurotoxicity via intraneuronal Zn(2+) release and a K(+) current surge. Glia 2008, 56: 89-96. 10.1002/glia.20592
  Article PubMed Central PubMed Google Scholar
• Qian L, Tan KS, Wei SJ, Wu HM, Xu Z, Wilson B, Lu RB, Hong JS, Flood PM: Microglia-mediated neurotoxicity is inhibited by morphine through an opioid receptor-independent reduction of NADPH oxidase activity. J Immunol 2007, 179: 1198-1209.
  Article CAS PubMed Google Scholar
• Diestel A, Troeller S, Billecke N, Sauer IM, Berger F, Schmitt KR: Mechanisms of hypothermia-induced cell protection mediated by microglial cells in vitro. Eur J Neurosci 2010, 31: 779-787. 10.1111/j.1460-9568.2010.07128.x
  Article PubMed Google Scholar
• Liang J, Takeuchi H, Jin S, Noda M, Li H, Doi Y, Kawanokuchi J, Sonobe Y, Mizuno T, Suzumura A: Glutamate induces neurotrophic factor production from microglia via protein kinase C pathway. Brain Res 2010, 1322: 8-23.
  Article CAS PubMed Google Scholar
• Walton NM, Sutter BM, Laywell ED, Levkoff LH, Kearns SM, Marshall GP, Scheffler B, Steindler DA: Microglia instruct subventricular zone neurogenesis. Glia 2006, 54: 815-825. 10.1002/glia.20419
  Article PubMed Google Scholar
• Thored P, Heldmann U, Gomes-Leal W, Gisler R, Darsalia V, Taneera J, Nygren JM, Jacobsen SE, Ekdahl CT, Kokaia Z, Lindvall O: Long-term accumulation of microglia with proneurogenic phenotype concomitant with persistent neurogenesis in adult subventricular zone after stroke. Glia 2009, 57: 835-849. 10.1002/glia.20810
  Article PubMed Google Scholar
• McPherson CA, Kraft AD, Harry GJ: Injury-induced neurogenesis: consideration of resident microglia as supportive of neural progenitor cells. Neurotox Res 2011, 19: 341-352. 10.1007/s12640-010-9199-6
  Article PubMed Central PubMed Google Scholar
• Sawada M, Sawada H, Nagatsu T: Effects of aging on neuroprotective and neurotoxic properties of microglia in neurodegenerative diseases. Neurodegener Dis 2008, 5: 254-256. 10.1159/000113717
  Article CAS PubMed Google Scholar
• Conde JR, Streit WJ: Effect of aging on the microglial response to peripheral nerve injury. Neurobiol Aging 2006, 27: 1451-1461. 10.1016/j.neurobiolaging.2005.07.012
  Article CAS PubMed Google Scholar
• Luo XG, Ding JQ, Chen SD: Microglia in the aging brain: relevance to neurodegeneration. Mol Neurodegener 2010, 5: 12. 10.1186/1750-1326-5-12
  Article PubMed Central PubMed Google Scholar
• Streit WJ, Sammons NW, Kuhns AJ, Sparks DL: Dystrophic microglia in the aging human brain. Glia 2004, 45: 208-212. 10.1002/glia.10319
  Article PubMed Google Scholar
• Wasserman JK, Yang H, Schlichter LC: Glial responses, neuron death and lesion resolution after intracerebral hemorrhage in young vs. aged rats. Eur J Neurosci 2008, 28: 1316-1328. 10.1111/j.1460-9568.2008.06442.x
  Article PubMed Google Scholar
• Flanary BE, Sammons NW, Nguyen C, Walker D, Streit WJ: Evidence that aging and amyloid promote microglial cell senescence. Rejuvenation Res 2007, 10: 61-74. 10.1089/rej.2006.9096
  Article CAS PubMed Google Scholar
• Sugama S, Yang L, Cho BP, DeGiorgio LA, Lorenzl S, Albers DS, Beal MF, Volpe BT, Joh TH: Age-related microglial activation in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced dopaminergic neurodegeneration in C57BL/6 mice. Brain Res 2003, 964: 288-294. 10.1016/S0006-8993(02)04085-4
  Article CAS PubMed Google Scholar
• Sandhir R, Onyszchuk G, Berman NE: Exacerbated glial response in the aged mouse hippocampus following controlled cortical impact injury. Exp Neurol 2008, 213: 372-380. 10.1016/j.expneurol.2008.06.013
  Article PubMed Central CAS PubMed Google Scholar
• Kyrkanides S, O’Banion MK, Whiteley PE, Daeschner JC, Olschowka JA: Enhanced glial activation and expression of specific CNS inflammation-related molecules in aged versus young rats following cortical stab injury. J Neuroimmunol 2001, 119: 269-277. 10.1016/S0165-5728(01)00404-0
  Article CAS PubMed Google Scholar
• Kim KY, Ju WK, Neufeld AH: Neuronal susceptibility to damage: comparison of the retinas of young, old and old/caloric restricted rats before and after transient ischemia. Neurobiol Aging 2004, 25: 491-500. 10.1016/j.neurobiolaging.2003.07.005
  Article CAS PubMed Google Scholar
• Lu W, Bhasin M, Tsirka SE: Involvement of tissue plasminogen activator in onset and effector phases of experimental allergic encephalomyelitis. J Neurosci 2002, 22: 10781-10789.
  PubMed Central CAS PubMed Google Scholar
• Bhasin M, Wu M, Tsirka SE: Modulation of microglial/macrophage activation by macrophage inhibitory factor (TKP) or tuftsin (TKPR) attenuates the disease course of experimental autoimmune encephalomyelitis. BMC Immunol 2007, 8: 10. 10.1186/1471-2172-8-10
  Article PubMed Central PubMed CAS Google Scholar
• El Khoury J, Toft M, Hickman SE, Means TK, Terada K, Geula C, Luster AD: Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat Med 2007, 13: 432-438. 10.1038/nm1555
  Article CAS PubMed Google Scholar
• Gordon S: Alternative activation of macrophages. Nat Rev Immunol 2003, 3: 23-35. 10.1038/nri978
  Article CAS PubMed Google Scholar
• Gordon S, Taylor PR: Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005, 5: 953-964. 10.1038/nri1733
  Article CAS PubMed Google Scholar
• Wynn TA, Thompson RW, Cheever AW, Mentink-Kane MM: Immunopathogenesis of schistosomiasis. Immunol Rev 2004, 201: 156-167. 10.1111/j.0105-2896.2004.00176.x
  Article CAS PubMed Google Scholar
• Herber DL, Mercer M, Roth LM, Symmonds K, Maloney J, Wilson N, Freeman MJ, Morgan D, Gordon MN: Microglial activation is required for Abeta clearance after intracranial injection of lipopolysaccharide in APP transgenic mice. J Neuroimmune Pharmacol 2007, 2: 222-231. 10.1007/s11481-007-9069-z
  Article PubMed Google Scholar
• Akiyama H: Inflammatory response in Alzheimer’s disease. Tohoku J Exp Med 1994, 174: 295-303. 10.1620/tjem.174.295
  Article CAS PubMed Google Scholar
• Ciaramella A, Bizzoni F, Salani F, Vanni D, Spalletta G, Sanarico N, Vendetti S, Caltagirone C, Bossu P: Increased pro-inflammatory response by dendritic cells from patients with Alzheimer’s disease. J Alzheimers Dis 2010, 19: 559-572.
  PubMed Google Scholar
• Rogers J: The inflammatory response in Alzheimer’s disease. J Periodontol 2008, 79: 1535-1543. 10.1902/jop.2008.080171
  Article CAS PubMed Google Scholar
• Colton CA, Mott RT, Sharpe H, Xu Q, Van Nostrand WE, Vitek MP: Expression profiles for macrophage alternative activation genes in AD and in mouse models of AD. J Neuroinflammation 2006, 3: 27. 10.1186/1742-2094-3-27
  Article PubMed Central PubMed CAS Google Scholar
• Sawada H, Suzuki H, Nagatsu T, Sawada M: Neuroprotective and neurotoxic phenotypes of activated microglia in neonatal mice with respective MPTP- and ethanol-induced brain injury. Neurodegener Dis 2010, 7: 64-67. 10.1159/000285508
  Article CAS PubMed Google Scholar
• Lai AY, Todd KG: Differential regulation of trophic and proinflammatory microglial effectors is dependent on severity of neuronal injury. Glia 2008, 56: 259-270. 10.1002/glia.20610
  Article PubMed Google Scholar
• Hald A, Nedergaard S, Hansen RR, Ding M, Heegaard AM: Differential activation of spinal cord glial cells in murine models of neuropathic and cancer pain. Eur J Pain 2009, 13: 138-145. 10.1016/j.ejpain.2008.03.014
  Article CAS PubMed Google Scholar
• Carson MJ, Reilly CR, Sutcliffe JG, Lo D: Mature microglia resemble immature antigen-presenting cells. Glia 1998, 22: 72-85. 10.1002/(SICI)1098-1136(199801)22:1<72::AID-GLIA7>3.0.CO;2-A
  Article CAS PubMed Google Scholar
• Ekdahl CT, Kokaia Z, Lindvall O: Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 2009, 158: 1021-1029. 10.1016/j.neuroscience.2008.06.052
  Article CAS PubMed Google Scholar
• Aarum J, Sandberg K, Haeberlein SL, Persson MA: Migration and differentiation of neural precursor cells can be directed by microglia. Proc Natl Acad Sci U S A 2003, 100: 15983-15988. 10.1073/pnas.2237050100
  Article PubMed Central CAS PubMed Google Scholar
• Luo X, Ge C, Ren Y, Zhou J, Li X, Yan R, Zhang C: BV2 enhanced the neurotrophic functions of mesenchymal stem cells after being stimulated with injured PC12. Neuroimmunomodulation 2009, 16: 28-34. 10.1159/000179664
  Article CAS PubMed Google Scholar
• Luo XG, Wang H, Zhou J, Yan R, Wu Z, Zhang CD, Wang QS: Beneficial effects of BV2 cell on proliferation and neuron-differentiating of mesenchymal stem cells in the circumstance of injured PC12 cell supernatant. Neurosci Bull 2006, 22: 221-226.
  CAS PubMed Google Scholar
• Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O: Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci U S A 2003, 100: 13632-13637. 10.1073/pnas.2234031100
  Article PubMed Central CAS PubMed Google Scholar
• Monje ML, Toda H, Palmer TD: Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003, 302: 1760-1765. 10.1126/science.1088417
  Article CAS PubMed Google Scholar
• Yang F, Liu ZR, Chen J, Zhang SJ, Quan QY, Huang YG, Jiang W: Roles of astrocytes and microglia in seizure-induced aberrant neurogenesis in the hippocampus of adult rats. J Neurosci Res 2010, 88: 519-529.
  Article CAS PubMed Google Scholar
• Monje ML, Mizumatsu S, Fike JR, Palmer TD: Irradiation induces neural precursor-cell dysfunction. Nat Med 2002, 8: 955-962. 10.1038/nm749
  Article CAS PubMed Google Scholar
• Battista D, Ferrari CC, Gage FH, Pitossi FJ: Neurogenic niche modulation by activated microglia: transforming growth factor beta increases neurogenesis in the adult dentate gyrus. Eur J Neurosci 2006, 23: 83-93. 10.1111/j.1460-9568.2005.04539.x
  Article PubMed Google Scholar
• Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, Pluchino S, Martino G, Schwartz M: Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 2006, 31: 149-160. 10.1016/j.mcn.2005.10.006
  Article CAS PubMed Google Scholar
• Aberg MA, Aberg ND, Palmer TD, Alborn AM, Carlsson-Skwirut C, Bang P, Rosengren LE, Olsson T, Gage FH, Eriksson PS: IGF-I has a direct proliferative effect in adult hippocampal progenitor cells. Mol Cell Neurosci 2003, 24: 23-40. 10.1016/S1044-7431(03)00082-4
  Article CAS PubMed Google Scholar
• Choi YS, Cho HY, Hoyt KR, Naegele JR, Obrietan K: IGF-1 receptor-mediated ERK/MAPK signaling couples status epilepticus to progenitor cell proliferation in the subgranular layer of the dentate gyrus. Glia 2008, 56: 791-800. 10.1002/glia.20653
  Article PubMed Central PubMed Google Scholar
• Butovsky O, Hauben E, Schwartz M: Morphological aspects of spinal cord autoimmune neuroprotection: colocalization of T cells with B7–2 (CD86) and prevention of cyst formation. Faseb J 2001, 15: 1065-1067.
  CAS PubMed Google Scholar
• Buckwalter MS, Yamane M, Coleman BS, Ormerod BK, Chin JT, Palmer T, Wyss-Coray T: Chronically increased transforming growth factor-beta1 strongly inhibits hippocampal neurogenesis in aged mice. Am J Pathol 2006, 169: 154-164. 10.2353/ajpath.2006.051272
  Article PubMed Central CAS PubMed Google Scholar
• Ogita K, Nishiyama N, Sugiyama C, Higuchi K, Yoneyama M, Yoneda Y: Regeneration of granule neurons after lesioning of hippocampal dentate gyrus: evaluation using adult mice treated with trimethyltin chloride as a model. J Neurosci Res 2005, 82: 609-621. 10.1002/jnr.20678
  Article CAS PubMed Google Scholar
• Harry GJ, McPherson CA, Wine RN, Atkinson K, Lefebvre d’Hellencourt C: Trimethyltin-induced neurogenesis in the murine hippocampus. Neurotox Res 2004, 5: 623-627.
  Article PubMed Central PubMed Google Scholar
• Kuhn HG, Dickinson-Anson H, Gage FH: Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 1996, 16: 2027-2033.
  CAS PubMed Google Scholar
• Knoth R, Singec I, Ditter M, Pantazis G, Capetian P, Meyer RP, Horvat V, Volk B, Kempermann G: Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS One 2010, 5: e8809. 10.1371/journal.pone.0008809
  Article PubMed Central PubMed CAS Google Scholar
• Zhu C, Qiu L, Wang X, Xu F, Nilsson M, Cooper-Kuhn C, Kuhn HG, Blomgren K: Age-dependent regenerative responses in the striatum and cortex after hypoxia-ischemia. J Cereb Blood Flow Metab 2009, 29: 342-354. 10.1038/jcbfm.2008.124
  Article CAS PubMed Google Scholar
• Ransohoff RM, Kivisakk P, Kidd G: Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 2003, 3: 569-581. 10.1038/nri1130
  Article CAS PubMed Google Scholar
• Ziv Y, Finkelstein A, Geffen Y, Kipnis J, Smirnov I, Shpilman S, Vertkin I, Kimron M, Lange A, Hecht T, et al.: A novel immune-based therapy for stroke induces neuroprotection and supports neurogenesis. Stroke 2007, 38: 774-782. 10.1161/01.STR.0000255784.27298.23
  Article CAS PubMed Google Scholar
• Ziv Y, Ron N, Butovsky O, Landa G, Sudai E, Greenberg N, Cohen H, Kipnis J, Schwartz M: Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 2006, 9: 268-275. 10.1038/nn1629
  Article CAS PubMed Google Scholar