Skip to main content
Erschienen in: Acta Neuropathologica 3/2014

01.09.2014 | Review

Microglia: unique and common features with other tissue macrophages

verfasst von: Marco Prinz, Tuan Leng Tay, Yochai Wolf, Steffen Jung

Erschienen in: Acta Neuropathologica | Ausgabe 3/2014

Einloggen, um Zugang zu erhalten

Abstract

Microglia are highly specialized tissue macrophages of the brain with dedicated functions in neuronal development, homeostasis and recovery from pathology Despite their unique localization in the central nervous system (CNS), microglia are ontogenetically and functionally related to their peripheral counterparts of the mononuclear phagocytic system in the body, namely tissue macrophages and circulating myeloid cells. Recent developments provided new insights into the myeloid system in the body with microglia emerging as intriguing unique archetypes. Similar to other tissue macrophages, microglia develop early during embryogenesis from immature yolk sac progenitors. But in contrast to most of their tissue relatives microglia persist throughout the entire life of the organism without any significant input from circulating blood cells due to their longevity and their capacity of self-renewal. Notably, microglia share some features with short-lived blood monocytes to limit CNS tissue damage in pathologies, but only bone marrow-derived cells display the ability to become permanently integrated in the parenchyma. This emphasizes the therapeutic potential of bone marrow-derived microglia-like cells. Further understanding of both fate and function of microglia during CNS pathologies and considering their uniqueness among other tissue macrophages will be pivotal for potential manipulation of immune cell function in the CNS, thereby reducing disease burden. Here, we discuss new aspects of myeloid cell biology in general with special emphasis on the brain-resident macrophages and microglia.
Literatur
1.
Zurück zum Zitat Abutbul S, Shapiro J, Szaingurten-Solodkin I et al (2012) TGF-β signaling through SMAD2/3 induces the quiescent microglial phenotype within the CNS environment. Glia 60:1160–1171. doi:10.1002/glia.22343 PubMed Abutbul S, Shapiro J, Szaingurten-Solodkin I et al (2012) TGF-β signaling through SMAD2/3 induces the quiescent microglial phenotype within the CNS environment. Glia 60:1160–1171. doi:10.​1002/​glia.​22343 PubMed
2.
Zurück zum Zitat Ajami B, Bennett JL, Krieger C et al (2007) Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 10:1538–1543. doi:10.1038/nn2014 PubMed Ajami B, Bennett JL, Krieger C et al (2007) Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 10:1538–1543. doi:10.​1038/​nn2014 PubMed
3.
Zurück zum Zitat Ajami B, Bennett JL, Krieger C et al (2011) Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat Neurosci 14:1142–1149. doi:10.1038/nn.2887 PubMed Ajami B, Bennett JL, Krieger C et al (2011) Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat Neurosci 14:1142–1149. doi:10.​1038/​nn.​2887 PubMed
5.
6.
Zurück zum Zitat Bauer S, Kerr BJ, Patterson PH (2007) The neuropoietic cytokine family in development, plasticity, disease and injury. Nat Rev Neurosci 8:221–232PubMed Bauer S, Kerr BJ, Patterson PH (2007) The neuropoietic cytokine family in development, plasticity, disease and injury. Nat Rev Neurosci 8:221–232PubMed
7.
Zurück zum Zitat Bechmann I, Priller J, Kovac A et al (2001) Immune surveillance of mouse brain perivascular spaces by blood-borne macrophages. Eur J Neurosci 14:1651–1658PubMed Bechmann I, Priller J, Kovac A et al (2001) Immune surveillance of mouse brain perivascular spaces by blood-borne macrophages. Eur J Neurosci 14:1651–1658PubMed
9.
Zurück zum Zitat Bialas AR, Stevens B (2013) TGF-β signaling regulates neuronal C1q expression and developmental synaptic refinement. Nat Neurosci 16:1–12. doi:10.1038/nn.3560 Bialas AR, Stevens B (2013) TGF-β signaling regulates neuronal C1q expression and developmental synaptic refinement. Nat Neurosci 16:1–12. doi:10.​1038/​nn.​3560
10.
Zurück zum Zitat Biber K, Neumann H, Inoue K, Boddeke H (2007) Neuronal ‘On’ and ‘Off’ signals control microglia. Trends Neurosci 30:596–602PubMed Biber K, Neumann H, Inoue K, Boddeke H (2007) Neuronal ‘On’ and ‘Off’ signals control microglia. Trends Neurosci 30:596–602PubMed
11.
13.
Zurück zum Zitat Cardona AE, Pioro EP, Sasse ME et al (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9:917–924. doi:10.1038/nn1715 PubMed Cardona AE, Pioro EP, Sasse ME et al (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9:917–924. doi:10.​1038/​nn1715 PubMed
14.
Zurück zum Zitat Cartier N, Hacein-Bey-Abina S, Bartholomae CC et al (2009) Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326:818–823. doi:10.1126/science.1171242 PubMed Cartier N, Hacein-Bey-Abina S, Bartholomae CC et al (2009) Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326:818–823. doi:10.​1126/​science.​1171242 PubMed
15.
Zurück zum Zitat Celada A, Borràs FE, Soler C et al (1996) The transcription factor PU.1 is involved in macrophage proliferation. J Exp Med 184:61–69PubMed Celada A, Borràs FE, Soler C et al (1996) The transcription factor PU.1 is involved in macrophage proliferation. J Exp Med 184:61–69PubMed
18.
Zurück zum Zitat Coull JAM, Beggs S, Boudreau D et al (2005) BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438:1017–1021. doi:10.1038/nature04223 PubMed Coull JAM, Beggs S, Boudreau D et al (2005) BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438:1017–1021. doi:10.​1038/​nature04223 PubMed
19.
20.
Zurück zum Zitat Davalos D, Grutzendler J, Yang G et al (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752–758. doi:10.1038/nn1472 PubMed Davalos D, Grutzendler J, Yang G et al (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752–758. doi:10.​1038/​nn1472 PubMed
21.
Zurück zum Zitat Davies LC, Rosas M, Smith PJ et al (2011) A quantifiable proliferative burst of tissue macrophages restores homeostatic macrophage populations after acute inflammation. Eur J Immunol 41:2155–2164. doi:10.1002/eji.201141817 PubMed Davies LC, Rosas M, Smith PJ et al (2011) A quantifiable proliferative burst of tissue macrophages restores homeostatic macrophage populations after acute inflammation. Eur J Immunol 41:2155–2164. doi:10.​1002/​eji.​201141817 PubMed
22.
Zurück zum Zitat Davies LC, Rosas M, Jenkins SJ et al (2013) Distinct bone marrow-derived and tissue-resident macrophage lineages proliferate at key stages during inflammation. Nat Commun 4:1886. doi:10.1038/ncomms2877 PubMed Davies LC, Rosas M, Jenkins SJ et al (2013) Distinct bone marrow-derived and tissue-resident macrophage lineages proliferate at key stages during inflammation. Nat Commun 4:1886. doi:10.​1038/​ncomms2877 PubMed
24.
Zurück zum Zitat Djukic M, Mildner A, Schmidt H et al (2006) Circulating monocytes engraft in the brain, differentiate into microglia and contribute to the pathology following meningitis in mice. Brain 129:2394–2403. doi:10.1093/brain/awl206 PubMed Djukic M, Mildner A, Schmidt H et al (2006) Circulating monocytes engraft in the brain, differentiate into microglia and contribute to the pathology following meningitis in mice. Brain 129:2394–2403. doi:10.​1093/​brain/​awl206 PubMed
25.
Zurück zum Zitat Dumser M, Bauer J, Lassmann H et al (2007) Lack of adrenoleukodystrophy protein enhances oligodendrocyte disturbance and microglia activation in mice with combined Abcd1/Mag deficiency. Acta Neuropathol 114:573–586. doi:10.1007/s00401-007-0288-4 PubMed Dumser M, Bauer J, Lassmann H et al (2007) Lack of adrenoleukodystrophy protein enhances oligodendrocyte disturbance and microglia activation in mice with combined Abcd1/Mag deficiency. Acta Neuropathol 114:573–586. doi:10.​1007/​s00401-007-0288-4 PubMed
27.
Zurück zum Zitat Epelman S, Lavine KJ, Beaudin AE et al (2014) Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 40:91–104. doi:10.1016/j.immuni.2013.11.019 PubMed Epelman S, Lavine KJ, Beaudin AE et al (2014) Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 40:91–104. doi:10.​1016/​j.​immuni.​2013.​11.​019 PubMed
30.
32.
Zurück zum Zitat Gautier EL, Shay T, Miller J et al (2012) Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol 13:1118–1128. doi:10.1038/ni.2419 PubMedCentralPubMed Gautier EL, Shay T, Miller J et al (2012) Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol 13:1118–1128. doi:10.​1038/​ni.​2419 PubMedCentralPubMed
33.
Zurück zum Zitat Geissmann F, Jung S, Littman DR (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19:71–82PubMed Geissmann F, Jung S, Littman DR (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19:71–82PubMed
36.
Zurück zum Zitat Gitik M, Liraz-Zaltsman S, Oldenborg P-A et al (2011) Myelin down-regulates myelin phagocytosis by microglia and macrophages through interactions between CD47 on myelin and SIRPα (signal regulatory protein-α) on phagocytes. J Neuroinflammation 8:24. doi:10.1186/1742-2094-8-24 PubMedCentralPubMed Gitik M, Liraz-Zaltsman S, Oldenborg P-A et al (2011) Myelin down-regulates myelin phagocytosis by microglia and macrophages through interactions between CD47 on myelin and SIRPα (signal regulatory protein-α) on phagocytes. J Neuroinflammation 8:24. doi:10.​1186/​1742-2094-8-24 PubMedCentralPubMed
38.
39.
Zurück zum Zitat Goldmann T, Wieghofer P, Müller PF et al (2013) A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat Neurosci 16:1618–1626. doi:10.1038/nn.3531 PubMed Goldmann T, Wieghofer P, Müller PF et al (2013) A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat Neurosci 16:1618–1626. doi:10.​1038/​nn.​3531 PubMed
43.
45.
Zurück zum Zitat Hamerman JA, Jarjoura JR, Humphrey MB et al (2006) Cutting edge: inhibition of TLR and FcR responses in macrophages by triggering receptor expressed on myeloid cells (TREM)-2 and DAP12. J Immunol 177:2051–2055PubMed Hamerman JA, Jarjoura JR, Humphrey MB et al (2006) Cutting edge: inhibition of TLR and FcR responses in macrophages by triggering receptor expressed on myeloid cells (TREM)-2 and DAP12. J Immunol 177:2051–2055PubMed
46.
Zurück zum Zitat Hanisch U-K, 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 PubMed Hanisch U-K, 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 PubMed
47.
48.
Zurück zum Zitat Heneka MT, Kummer MP, Stutz A et al (2012) NLRP3 is activated in Alzheimer’s disease and contributes to pathology in APP/PS1 mice. Nature 493:674–678. doi:10.1038/nature11729 PubMed Heneka MT, Kummer MP, Stutz A et al (2012) NLRP3 is activated in Alzheimer’s disease and contributes to pathology in APP/PS1 mice. Nature 493:674–678. doi:10.​1038/​nature11729 PubMed
49.
Zurück zum Zitat Herbomel P, Thisse B, Thisse C (1999) Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126:3735–3745PubMed Herbomel P, Thisse B, Thisse C (1999) Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126:3735–3745PubMed
50.
Zurück zum Zitat Hickey WF, Kimura H (1988) Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 239:290–292PubMed Hickey WF, Kimura H (1988) Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 239:290–292PubMed
51.
Zurück zum Zitat Hickman SE, Kingery ND, Ohsumi TK et al (2013) The microglial sensome revealed by direct RNA sequencing. Nat Neurosci 16:1896–1905. doi:10.1038/nn.3554 PubMed Hickman SE, Kingery ND, Ohsumi TK et al (2013) The microglial sensome revealed by direct RNA sequencing. Nat Neurosci 16:1896–1905. doi:10.​1038/​nn.​3554 PubMed
52.
Zurück zum Zitat Hoeffel G, Wang Y, Greter M et al (2012) Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sac-derived macrophages. J Exp Med 209:1167–1181. doi:10.1084/jem.20120340 PubMedCentralPubMed Hoeffel G, Wang Y, Greter M et al (2012) Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sac-derived macrophages. J Exp Med 209:1167–1181. doi:10.​1084/​jem.​20120340 PubMedCentralPubMed
54.
Zurück zum Zitat Hoshiko M, Arnoux I, Avignone E et al (2012) Deficiency of the microglial receptor CX3CR1 impairs postnatal functional development of thalamocortical synapses in the barrel cortex. J Neurosci 32:15106–15111. doi:10.1523/JNEUROSCI.1167-12.2012 PubMed Hoshiko M, Arnoux I, Avignone E et al (2012) Deficiency of the microglial receptor CX3CR1 impairs postnatal functional development of thalamocortical synapses in the barrel cortex. J Neurosci 32:15106–15111. doi:10.​1523/​JNEUROSCI.​1167-12.​2012 PubMed
55.
Zurück zum Zitat Jovicic A, Roshan R, Moisoi N et al (2013) Comprehensive expression analyses of neural cell-type-specific miRNAs identify new determinants of the specification and maintenance of neuronal phenotypes. J Neurosci 33:5127–5137. doi:10.1523/JNEUROSCI.0600-12.2013 PubMed Jovicic A, Roshan R, Moisoi N et al (2013) Comprehensive expression analyses of neural cell-type-specific miRNAs identify new determinants of the specification and maintenance of neuronal phenotypes. J Neurosci 33:5127–5137. doi:10.​1523/​JNEUROSCI.​0600-12.​2013 PubMed
58.
Zurück zum Zitat Kierdorf K, Erny D, Goldmann T et al (2013) Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat Neurosci 16:273–280. doi:10.1038/nn.3318 PubMed Kierdorf K, Erny D, Goldmann T et al (2013) Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat Neurosci 16:273–280. doi:10.​1038/​nn.​3318 PubMed
63.
Zurück zum Zitat Kurz H, Christ B (1998) Embryonic CNS macrophages and microglia do not stem from circulating, but from extravascular precursors. Glia 22:98–102PubMed Kurz H, Christ B (1998) Embryonic CNS macrophages and microglia do not stem from circulating, but from extravascular precursors. Glia 22:98–102PubMed
64.
Zurück zum Zitat Lagasse E, Weissman IL (1996) Flow cytometric identification of murine neutrophils and monocytes. J Immunol Methods 197:139–150PubMed Lagasse E, Weissman IL (1996) Flow cytometric identification of murine neutrophils and monocytes. J Immunol Methods 197:139–150PubMed
65.
Zurück zum Zitat Lambertsen KL, Deierborg T, Gregersen R et al (2011) Differences in origin of reactive microglia in bone marrow chimeric mouse and rat after transient global ischemia. J Neuropathol Exp Neurol 70:481–494. doi:10.1097/NEN.0b013e31821db3aa PubMed Lambertsen KL, Deierborg T, Gregersen R et al (2011) Differences in origin of reactive microglia in bone marrow chimeric mouse and rat after transient global ischemia. J Neuropathol Exp Neurol 70:481–494. doi:10.​1097/​NEN.​0b013e31821db3aa​ PubMed
66.
Zurück zum Zitat Lampron A, Pimentel-Coelho PM, Rivest S (2013) Migration of bone marrow-derived cells into the central nervous system in models of neurodegeneration. J Comp Neurol 521:3863–3876. doi:10.1002/cne.23363 PubMed Lampron A, Pimentel-Coelho PM, Rivest S (2013) Migration of bone marrow-derived cells into the central nervous system in models of neurodegeneration. J Comp Neurol 521:3863–3876. doi:10.​1002/​cne.​23363 PubMed
68.
Zurück zum Zitat Lawson LJ, Perry VH, Gordon S (1992) Turnover of resident microglia in the normal adult mouse brain. Neuroscience 48:405–415PubMed Lawson LJ, Perry VH, Gordon S (1992) Turnover of resident microglia in the normal adult mouse brain. Neuroscience 48:405–415PubMed
69.
71.
72.
Zurück zum Zitat Liu Y, Teige I, Birnir B, Issazadeh-Navikas S (2006) Neuron-mediated generation of regulatory T cells from encephalitogenic T cells suppresses EAE. Nat Med 12:518–525. doi:10.1038/nm1402 PubMed Liu Y, Teige I, Birnir B, Issazadeh-Navikas S (2006) Neuron-mediated generation of regulatory T cells from encephalitogenic T cells suppresses EAE. Nat Med 12:518–525. doi:10.​1038/​nm1402 PubMed
73.
Zurück zum Zitat Marín-Teva JL, Dusart I, Colin C et al (2004) Microglia promote the death of developing Purkinje cells. Neuron 41:535–547PubMed Marín-Teva JL, Dusart I, Colin C et al (2004) Microglia promote the death of developing Purkinje cells. Neuron 41:535–547PubMed
76.
Zurück zum Zitat Matsumoto Y, Fujiwara M (1987) Absence of donor-type major histocompatibility complex class I antigen-bearing microglia in the rat central nervous system of radiation bone marrow chimeras. J Neuroimmunol 17:71–82PubMed Matsumoto Y, Fujiwara M (1987) Absence of donor-type major histocompatibility complex class I antigen-bearing microglia in the rat central nervous system of radiation bone marrow chimeras. J Neuroimmunol 17:71–82PubMed
77.
Zurück zum Zitat McKercher SR, Torbett BE, Anderson KL et al (1996) Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J 15:5647–5658PubMedCentralPubMed McKercher SR, Torbett BE, Anderson KL et al (1996) Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J 15:5647–5658PubMedCentralPubMed
78.
Zurück zum Zitat Michaelson MD, Bieri PL, Mehler MF et al (1996) CSF-1 deficiency in mice results in abnormal brain development. Development 122:2661–2672PubMed Michaelson MD, Bieri PL, Mehler MF et al (1996) CSF-1 deficiency in mice results in abnormal brain development. Development 122:2661–2672PubMed
79.
Zurück zum Zitat Mildner A, Schmidt H, Nitsche M et al (2007) Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci 10:1544–1553. doi:10.1038/nn2015 PubMed Mildner A, Schmidt H, Nitsche M et al (2007) Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci 10:1544–1553. doi:10.​1038/​nn2015 PubMed
80.
Zurück zum Zitat Mildner A, Djukic M, Garbe D et al (2008) Ly-6G + CCR2- myeloid cells rather than Ly-6ChighCCR2+ monocytes are required for the control of bacterial infection in the central nervous system. J Immunol 181:2713–2722PubMed Mildner A, Djukic M, Garbe D et al (2008) Ly-6G + CCR2- myeloid cells rather than Ly-6ChighCCR2+ monocytes are required for the control of bacterial infection in the central nervous system. J Immunol 181:2713–2722PubMed
81.
Zurück zum Zitat Mildner A, Mack M, Schmidt H et al (2009) CCR2+ Ly-6Chi monocytes are crucial for the effector phase of autoimmunity in the central nervous system. Brain 132:2487–2500. doi:10.1093/brain/awp144 PubMed Mildner A, Mack M, Schmidt H et al (2009) CCR2+ Ly-6Chi monocytes are crucial for the effector phase of autoimmunity in the central nervous system. Brain 132:2487–2500. doi:10.​1093/​brain/​awp144 PubMed
85.
Zurück zum Zitat Mizrahi A (2007) Dendritic development and plasticity of adult-born neurons in the mouse olfactory bulb. Nat Neurosci 10:444–452. doi:10.1038/nn1875 PubMed Mizrahi A (2007) Dendritic development and plasticity of adult-born neurons in the mouse olfactory bulb. Nat Neurosci 10:444–452. doi:10.​1038/​nn1875 PubMed
88.
Zurück zum Zitat Moran LB, Graeber MB (2004) The facial nerve axotomy model. Brain Res Brain Res Rev 44:154–178PubMed Moran LB, Graeber MB (2004) The facial nerve axotomy model. Brain Res Brain Res Rev 44:154–178PubMed
95.
Zurück zum Zitat Otero K, Turnbull IR, Poliani PL et al (2009) Macrophage colony-stimulating factor induces the proliferation and survival of macrophages via a pathway involving DAP12 and β-catenin. Nat Immunol 10:734–743. doi:10.1038/ni.1744 PubMedCentralPubMed Otero K, Turnbull IR, Poliani PL et al (2009) Macrophage colony-stimulating factor induces the proliferation and survival of macrophages via a pathway involving DAP12 and β-catenin. Nat Immunol 10:734–743. doi:10.​1038/​ni.​1744 PubMedCentralPubMed
96.
Zurück zum Zitat Paloneva J, Kestilä M, Wu J et al (2000) Loss-of-function mutations in TYROBP (DAP12) result in a presenile dementia with bone cysts. Nat Genet 25:357–361. doi:10.1038/77153 PubMed Paloneva J, Kestilä M, Wu J et al (2000) Loss-of-function mutations in TYROBP (DAP12) result in a presenile dementia with bone cysts. Nat Genet 25:357–361. doi:10.​1038/​77153 PubMed
100.
102.
Zurück zum Zitat Ponomarev ED, Veremeyko T, Barteneva N et al (2011) MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-α-PU.1 pathway. Nat Med 17:64–70. doi:10.1038/nm.2266 PubMedCentralPubMed Ponomarev ED, Veremeyko T, Barteneva N et al (2011) MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-α-PU.1 pathway. Nat Med 17:64–70. doi:10.​1038/​nm.​2266 PubMedCentralPubMed
103.
Zurück zum Zitat Priller J, Flügel A, Wehner T et al (2001) Targeting gene-modified hematopoietic cells to the central nervous system: use of green fluorescent protein uncovers microglial engraftment. Nat Med 7:1356–1361. doi:10.1038/nm1201-1356 PubMed Priller J, Flügel A, Wehner T et al (2001) Targeting gene-modified hematopoietic cells to the central nervous system: use of green fluorescent protein uncovers microglial engraftment. Nat Med 7:1356–1361. doi:10.​1038/​nm1201-1356 PubMed
104.
Zurück zum Zitat Prinz M, Priller J, Sisodia SS, Ransohoff RM (2011) Heterogeneity of CNS myeloid cells and their roles in neurodegeneration. Nat Neurosci 14:1227–1235. doi:10.1038/nn.2923 PubMed Prinz M, Priller J, Sisodia SS, Ransohoff RM (2011) Heterogeneity of CNS myeloid cells and their roles in neurodegeneration. Nat Neurosci 14:1227–1235. doi:10.​1038/​nn.​2923 PubMed
105.
Zurück zum Zitat Radjavi A, Smirnov I, Derecki N, Kipnis J (2013) Dynamics of the meningeal CD4(+) T-cell repertoire are defined by the cervical lymph nodes and facilitate cognitive task performance in mice. Mol Psychiatry. doi:10.1038/mp.2013.79 PubMed Radjavi A, Smirnov I, Derecki N, Kipnis J (2013) Dynamics of the meningeal CD4(+) T-cell repertoire are defined by the cervical lymph nodes and facilitate cognitive task performance in mice. Mol Psychiatry. doi:10.​1038/​mp.​2013.​79 PubMed
108.
110.
Zurück zum Zitat Rosenbauer F, Tenen DG (2007) Transcription factors in myeloid development: balancing differentiation with transformation. Nat Rev Immunol 7:105–117. doi:10.1038/nri2024 PubMed Rosenbauer F, Tenen DG (2007) Transcription factors in myeloid development: balancing differentiation with transformation. Nat Rev Immunol 7:105–117. doi:10.​1038/​nri2024 PubMed
113.
117.
Zurück zum Zitat Schwartz M, Butovsky O, Bruck W, Hanisch UK (2006) Microglial phenotype: is the commitment reversible? Trends Neurosci 29:68–74PubMed Schwartz M, Butovsky O, Bruck W, Hanisch UK (2006) Microglial phenotype: is the commitment reversible? Trends Neurosci 29:68–74PubMed
118.
Zurück zum Zitat Serbina NV, Pamer EG (2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 7:311–317. doi:10.1038/ni1309 PubMed Serbina NV, Pamer EG (2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 7:311–317. doi:10.​1038/​ni1309 PubMed
119.
Zurück zum Zitat Sessa G, Podini P, Mariani M et al (2004) Distribution and signaling of TREM2/DAP12, the receptor system mutated in human polycystic lipomembraneous osteodysplasia with sclerosing leukoencephalopathy dementia. Eur J Neurosci 20:2617–2628. doi:10.1111/j.1460-9568.2004.03729.x PubMed Sessa G, Podini P, Mariani M et al (2004) Distribution and signaling of TREM2/DAP12, the receptor system mutated in human polycystic lipomembraneous osteodysplasia with sclerosing leukoencephalopathy dementia. Eur J Neurosci 20:2617–2628. doi:10.​1111/​j.​1460-9568.​2004.​03729.​x PubMed
124.
Zurück zum Zitat Soulas C, Donahue RE, Dunbar CE et al (2009) Genetically modified CD34 + hematopoietic stem cells contribute to turnover of brain perivascular macrophages in long-term repopulated primates. Amer J Pathol 174:1808–1817. doi:10.2353/ajpath.2009.081010 Soulas C, Donahue RE, Dunbar CE et al (2009) Genetically modified CD34 + hematopoietic stem cells contribute to turnover of brain perivascular macrophages in long-term repopulated primates. Amer J Pathol 174:1808–1817. doi:10.​2353/​ajpath.​2009.​081010
125.
Zurück zum Zitat Stanley ER, Guilbert LJ, Tushinski RJ (1983) CSF-1—a mononuclear phagocyte lineage-specific hemopoietic growth factor. J Cell Biochem 21:151–159PubMed Stanley ER, Guilbert LJ, Tushinski RJ (1983) CSF-1—a mononuclear phagocyte lineage-specific hemopoietic growth factor. J Cell Biochem 21:151–159PubMed
126.
Zurück zum Zitat Stevens B, Allen NJ, Vazquez LE, Howell GR (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131:1164–1178PubMed Stevens B, Allen NJ, Vazquez LE, Howell GR (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131:1164–1178PubMed
128.
129.
Zurück zum Zitat Tamoutounour S, Guilliams M, Montanana Sanchis F et al (2013) Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity 39:925–938. doi:10.1016/j.immuni.2013.10.004 PubMed Tamoutounour S, Guilliams M, Montanana Sanchis F et al (2013) Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity 39:925–938. doi:10.​1016/​j.​immuni.​2013.​10.​004 PubMed
132.
Zurück zum Zitat Turnbull IR, Gilfillan S, Cella M et al (2006) Cutting edge: TREM-2 attenuates macrophage activation. J Immunol 177:3520–3524PubMed Turnbull IR, Gilfillan S, Cella M et al (2006) Cutting edge: TREM-2 attenuates macrophage activation. J Immunol 177:3520–3524PubMed
133.
Zurück zum Zitat Ueno M, Fujita Y, Tanaka T et al (2013) Layer V cortical neurons require microglial support for survival during postnatal development. Nat Neurosci 16:543–551. doi:10.1038/nn.3358 PubMed Ueno M, Fujita Y, Tanaka T et al (2013) Layer V cortical neurons require microglial support for survival during postnatal development. Nat Neurosci 16:543–551. doi:10.​1038/​nn.​3358 PubMed
134.
Zurück zum Zitat Unger ER, Sung JH, Manivel JC et al (1993) Male donor-derived cells in the brains of female sex-mismatched bone marrow transplant recipients: a Y-chromosome specific in situ hybridization study. J Neuropathol Exp Neurol 52:460–470PubMed Unger ER, Sung JH, Manivel JC et al (1993) Male donor-derived cells in the brains of female sex-mismatched bone marrow transplant recipients: a Y-chromosome specific in situ hybridization study. J Neuropathol Exp Neurol 52:460–470PubMed
135.
Zurück zum Zitat Vallières L, Campbell IL, Gage FH, Sawchenko PE (2002) Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J Neurosci 22:486–492PubMed Vallières L, Campbell IL, Gage FH, Sawchenko PE (2002) Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J Neurosci 22:486–492PubMed
136.
138.
142.
Metadaten
Titel
Microglia: unique and common features with other tissue macrophages
verfasst von
Marco Prinz
Tuan Leng Tay
Yochai Wolf
Steffen Jung
Publikationsdatum
01.09.2014
Verlag
Springer Berlin Heidelberg
Erschienen in
Acta Neuropathologica / Ausgabe 3/2014
Print ISSN: 0001-6322
Elektronische ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-014-1267-1

Weitere Artikel der Ausgabe 3/2014

Acta Neuropathologica 3/2014 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.