Skip to main content
Erschienen in: Acta Neuropathologica 3/2017

06.07.2017 | Original Paper

Microglia contribute to normal myelinogenesis and to oligodendrocyte progenitor maintenance during adulthood

verfasst von: Nora Hagemeyer, Klara-Maria Hanft, Maria-Anna Akriditou, Nicole Unger, Eun S. Park, E. Richard Stanley, Ori Staszewski, Leda Dimou, Marco Prinz

Erschienen in: Acta Neuropathologica | Ausgabe 3/2017

Einloggen, um Zugang zu erhalten

Abstract

Whereas microglia involvement in virtually all brain diseases is well accepted their role in the control of homeostasis in the central nervous system (CNS) is mainly thought to be the maintenance of neuronal function through the formation, refinement, and monitoring of synapses in both the developing and adult brain. Although the prenatal origin as well as the neuron-centered function of cortical microglia has recently been elucidated, much less is known about a distinct amoeboid microglia population formerly described as the “fountain of microglia” that appears only postnatally in myelinated regions such as corpus callosum and cerebellum. Using large-scale transcriptional profiling, fate mapping, and genetic targeting approaches, we identified a unique molecular signature of this microglia subset that arose from a CNS endogenous microglia pool independent from circulating myeloid cells. Microglia depletion experiments revealed an essential role of postnatal microglia for the proper development and homeostasis of oligodendrocytes and their progenitors. Our data provide new cellular and molecular insights into the myelin-supporting function of microglia in the normal CNS.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Amit I, Winter DR, Jung S (2016) The role of the local environment and epigenetics in shaping macrophage identity and their effect on tissue homeostasis. Nat Immunol 17:18–25CrossRefPubMed Amit I, Winter DR, Jung S (2016) The role of the local environment and epigenetics in shaping macrophage identity and their effect on tissue homeostasis. Nat Immunol 17:18–25CrossRefPubMed
3.
Zurück zum Zitat Bruttger J, Karram K, Wörtge S, Regen T, Marini F, Hoppmann N, Klein M, Blank T, Yona S, Wolf Y, Mack M, Pinteaux E, Müller W, Zipp F, Binder H, Bopp T, Prinz M, Jung S, Waisman A (2015) Genetic cell ablation reveals clusters of local self-renewing microglia in the mammalian central nervous system. Immunity 43:92–106. doi:10.1016/j.immuni.2015.06.012 CrossRefPubMed Bruttger J, Karram K, Wörtge S, Regen T, Marini F, Hoppmann N, Klein M, Blank T, Yona S, Wolf Y, Mack M, Pinteaux E, Müller W, Zipp F, Binder H, Bopp T, Prinz M, Jung S, Waisman A (2015) Genetic cell ablation reveals clusters of local self-renewing microglia in the mammalian central nervous system. Immunity 43:92–106. doi:10.​1016/​j.​immuni.​2015.​06.​012 CrossRefPubMed
4.
Zurück zum Zitat Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, Pluchino S, Martino G, Schwartz M (2006) Microglia activated by IL-4 or IFN-γ differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 31:149–160. doi:10.1016/j.mcn.2005.10.006 CrossRefPubMed Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, Pluchino S, Martino G, Schwartz M (2006) Microglia activated by IL-4 or IFN-γ differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 31:149–160. doi:10.​1016/​j.​mcn.​2005.​10.​006 CrossRefPubMed
7.
Zurück zum Zitat De Jager PL, Jia X, Wang J, de Bakker PIW, Ottoboni L, Aggarwal NT, Piccio L, Raychaudhuri S, Tran D, Aubin C, Briskin R, Romano S, Baranzini SE, McCauley JL, Pericak-Vance MA, Haines JL, Gibson RA, Naeglin Y, Uitdehaag B, Matthews PM, Kappos L, Polman C, McArdle WL, Strachan DP, Evans D, Cross AH, Daly MJ, Compston A, Sawcer SJ, Weiner HL, Hauser SL, Hafler DA, Oksenberg JR (2009) Meta-analysis of genome scans and replication identify CD6, IRF8 and TNFRSF1A as new multiple sclerosis susceptibility loci. Nat Genet 41:776–782. doi:10.1038/ng.401 CrossRefPubMedPubMedCentral De Jager PL, Jia X, Wang J, de Bakker PIW, Ottoboni L, Aggarwal NT, Piccio L, Raychaudhuri S, Tran D, Aubin C, Briskin R, Romano S, Baranzini SE, McCauley JL, Pericak-Vance MA, Haines JL, Gibson RA, Naeglin Y, Uitdehaag B, Matthews PM, Kappos L, Polman C, McArdle WL, Strachan DP, Evans D, Cross AH, Daly MJ, Compston A, Sawcer SJ, Weiner HL, Hauser SL, Hafler DA, Oksenberg JR (2009) Meta-analysis of genome scans and replication identify CD6, IRF8 and TNFRSF1A as new multiple sclerosis susceptibility loci. Nat Genet 41:776–782. doi:10.​1038/​ng.​401 CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Elmore MRP, Najafi AR, Koike MA, Dagher NN, Spangenberg EE, Rice RA, Kitazawa M, Matusow B, Nguyen H, West BL, Green KN (2014) Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron 82:380–397. doi:10.1016/j.neuron.2014.02.040 CrossRefPubMedPubMedCentral Elmore MRP, Najafi AR, Koike MA, Dagher NN, Spangenberg EE, Rice RA, Kitazawa M, Matusow B, Nguyen H, West BL, Green KN (2014) Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron 82:380–397. doi:10.​1016/​j.​neuron.​2014.​02.​040 CrossRefPubMedPubMedCentral
9.
Zurück zum Zitat Ensan S, Li A, Besla R, Degousee N, Cosme J, Roufaiel M, Shikatani EA, El-Maklizi M, Williams JW, Robins L, Li C, Lewis B, Yun TJ, Lee JS, Wieghofer P, Khattar R, Farrokhi K, Byrne J, Ouzounian M, Zavitz CCJ, Levy GA, Bauer CMT, Libby P, Husain M, Swirski FK, Cheong C, Prinz M, Hilgendorf I, Randolph GJ, Epelman S, Gramolini AO, Cybulsky MI, Rubin BB, Robbins CS (2016) Self-renewing resident arterial macrophages arise from embryonic CX3CR1+ precursors and circulating monocytes immediately after birth. Nat Immunol 17:159–168CrossRefPubMed Ensan S, Li A, Besla R, Degousee N, Cosme J, Roufaiel M, Shikatani EA, El-Maklizi M, Williams JW, Robins L, Li C, Lewis B, Yun TJ, Lee JS, Wieghofer P, Khattar R, Farrokhi K, Byrne J, Ouzounian M, Zavitz CCJ, Levy GA, Bauer CMT, Libby P, Husain M, Swirski FK, Cheong C, Prinz M, Hilgendorf I, Randolph GJ, Epelman S, Gramolini AO, Cybulsky MI, Rubin BB, Robbins CS (2016) Self-renewing resident arterial macrophages arise from embryonic CX3CR1+ precursors and circulating monocytes immediately after birth. Nat Immunol 17:159–168CrossRefPubMed
11.
Zurück zum Zitat Erny D, Hrabe de Angelis AL, Jaitin D, Wieghofer P, Staszewski O, David E, Keren-Shaul H, Mahlakoiv T, Jakobshagen K, Buch T, Schwierzeck V, Utermohlen O, Chun E, Garrett WS, McCoy KD, Diefenbach A, Staeheli P, Stecher B, Amit I, Prinz M (2015) Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci 18:965–977CrossRefPubMedPubMedCentral Erny D, Hrabe de Angelis AL, Jaitin D, Wieghofer P, Staszewski O, David E, Keren-Shaul H, Mahlakoiv T, Jakobshagen K, Buch T, Schwierzeck V, Utermohlen O, Chun E, Garrett WS, McCoy KD, Diefenbach A, Staeheli P, Stecher B, Amit I, Prinz M (2015) Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci 18:965–977CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat Frank S, Burbach GJ, Bonin M, Walter M, Streit W, Bechmann I, Deller T (2008) TREM2 is upregulated in amyloid plaque-associated microglia in aged APP23 transgenic mice. Glia 56:1438–1447. doi:10.1002/glia.20710 CrossRefPubMed Frank S, Burbach GJ, Bonin M, Walter M, Streit W, Bechmann I, Deller T (2008) TREM2 is upregulated in amyloid plaque-associated microglia in aged APP23 transgenic mice. Glia 56:1438–1447. doi:10.​1002/​glia.​20710 CrossRefPubMed
13.
14.
Zurück zum Zitat Goldmann T, Wieghofer P, Jordao MJC, Prutek F, Hagemeyer N, Frenzel K, Amann L, Staszewski O, Kierdorf K, Krueger M, Locatelli G, Hochgerner H, Zeiser R, Epelman S, Geissmann F, Priller J, Rossi FMV, Bechmann I, Kerschensteiner M, Linnarsson S, Jung S, Prinz M (2016) Origin, fate and dynamics of macrophages at central nervous system interfaces. Nat Immunol 17:797–805CrossRefPubMedPubMedCentral Goldmann T, Wieghofer P, Jordao MJC, Prutek F, Hagemeyer N, Frenzel K, Amann L, Staszewski O, Kierdorf K, Krueger M, Locatelli G, Hochgerner H, Zeiser R, Epelman S, Geissmann F, Priller J, Rossi FMV, Bechmann I, Kerschensteiner M, Linnarsson S, Jung S, Prinz M (2016) Origin, fate and dynamics of macrophages at central nervous system interfaces. Nat Immunol 17:797–805CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Goldmann T, Zeller N, Raasch J, Kierdorf K, Frenzel K, Ketscher L, Basters A, Staszewski O, Brendecke SM, Spiess A, Tay TL, Kreutz C, Timmer J, Mancini GM, Blank T, Fritz G, Biber K, Lang R, Malo D, Merkler D, Heikenwälder M, Knobeloch K-P, Prinz M (2015) USP18 lack in microglia causes destructive interferonopathy of the mouse brain. EMBO J 34:1612–1629. doi:10.15252/embj.201490791 CrossRefPubMedPubMedCentral Goldmann T, Zeller N, Raasch J, Kierdorf K, Frenzel K, Ketscher L, Basters A, Staszewski O, Brendecke SM, Spiess A, Tay TL, Kreutz C, Timmer J, Mancini GM, Blank T, Fritz G, Biber K, Lang R, Malo D, Merkler D, Heikenwälder M, Knobeloch K-P, Prinz M (2015) USP18 lack in microglia causes destructive interferonopathy of the mouse brain. EMBO J 34:1612–1629. doi:10.​15252/​embj.​201490791 CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Grabert K, Michoel T, Karavolos MH, Clohisey S, Baillie JK, Stevens MP, Freeman TC, Summers KM, McColl BW (2016) Microglial brain region-dependent diversity and selective regional sensitivities to aging. Nat Neurosci 19:504–516CrossRefPubMedPubMedCentral Grabert K, Michoel T, Karavolos MH, Clohisey S, Baillie JK, Stevens MP, Freeman TC, Summers KM, McColl BW (2016) Microglial brain region-dependent diversity and selective regional sensitivities to aging. Nat Neurosci 19:504–516CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat Guerreiro R, Wojtas A, Bras J, Carrasquillo M, Rogaeva E, Majounie E, Cruchaga C, Sassi C, Kauwe JSK, Younkin S, Hazrati L, Collinge J, Pocock J, Lashley T, Williams J, Lambert J-C, Amouyel P, Goate A, Rademakers R, Morgan K, Powell J, St. George-Hyslop P, Singleton A, Hardy J (2012) TREM2 Variants in Alzheimer’s Disease. N Engl J Med 368:117–127. doi:10.1056/NEJMoa1211851 CrossRefPubMedPubMedCentral Guerreiro R, Wojtas A, Bras J, Carrasquillo M, Rogaeva E, Majounie E, Cruchaga C, Sassi C, Kauwe JSK, Younkin S, Hazrati L, Collinge J, Pocock J, Lashley T, Williams J, Lambert J-C, Amouyel P, Goate A, Rademakers R, Morgan K, Powell J, St. George-Hyslop P, Singleton A, Hardy J (2012) TREM2 Variants in Alzheimer’s Disease. N Engl J Med 368:117–127. doi:10.​1056/​NEJMoa1211851 CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Hagemeyer N, Goebbels S, Papiol S, Kästner A, Hofer S, Begemann M, Gerwig UC, Boretius S, Wieser GL, Ronnenberg A, Gurvich A, Heckers SH, Frahm J, Nave K-A, Ehrenreich H (2012) A myelin gene causative of a catatonia-depression syndrome upon aging. EMBO Mol Med 4:528–539. doi:10.1002/emmm.201200230 CrossRefPubMedPubMedCentral Hagemeyer N, Goebbels S, Papiol S, Kästner A, Hofer S, Begemann M, Gerwig UC, Boretius S, Wieser GL, Ronnenberg A, Gurvich A, Heckers SH, Frahm J, Nave K-A, Ehrenreich H (2012) A myelin gene causative of a catatonia-depression syndrome upon aging. EMBO Mol Med 4:528–539. doi:10.​1002/​emmm.​201200230 CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Hagemeyer N, Kierdorf K, Frenzel K, Xue J, Ringelhan M, Abdullah Z, Godin I, Wieghofer P, Costa Jordão MJ, Ulas T, Yorgancioglu G, Rosenbauer F, Knolle PA, Heikenwalder M, Schultze JL, Prinz M (2016) Transcriptome-based profiling of yolk sac-derived macrophages reveals a role for Irf8 in macrophage maturation. EMBO J 35:1730–1744. doi:10.15252/embj.201693801 CrossRefPubMedPubMedCentral Hagemeyer N, Kierdorf K, Frenzel K, Xue J, Ringelhan M, Abdullah Z, Godin I, Wieghofer P, Costa Jordão MJ, Ulas T, Yorgancioglu G, Rosenbauer F, Knolle PA, Heikenwalder M, Schultze JL, Prinz M (2016) Transcriptome-based profiling of yolk sac-derived macrophages reveals a role for Irf8 in macrophage maturation. EMBO J 35:1730–1744. doi:10.​15252/​embj.​201693801 CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Hollingworth P, Harold D, Sims R, Gerrish A, Lambert J-C, Carrasquillo MM, Abraham R, Hamshere ML, Pahwa JS, Moskvina V, Dowzell K, Jones N, Stretton A, Thomas C, Richards A et al (2011) Common variants at ABCA7, MS4A6A/MS4A4E, EPHA1, CD33 and CD2AP are associated with Alzheimer’s disease. Nat Genet 43:429–435. doi:10.1038/ng.803 CrossRefPubMedPubMedCentral Hollingworth P, Harold D, Sims R, Gerrish A, Lambert J-C, Carrasquillo MM, Abraham R, Hamshere ML, Pahwa JS, Moskvina V, Dowzell K, Jones N, Stretton A, Thomas C, Richards A et al (2011) Common variants at ABCA7, MS4A6A/MS4A4E, EPHA1, CD33 and CD2AP are associated with Alzheimer’s disease. Nat Genet 43:429–435. doi:10.​1038/​ng.​803 CrossRefPubMedPubMedCentral
23.
Zurück zum Zitat Holtman IR, Raj DD, Miller JA, Schaafsma W, Yin Z, Brouwer N, Wes PD, Möller T, Orre M, Kamphuis W, Hol EM, Boddeke EWGM, Eggen BJL (2015) Induction of a common microglia gene expression signature by aging and neurodegenerative conditions: a co-expression meta-analysis. Acta Neuropathol Commun 3:31. doi:10.1186/s40478-015-0203-5 CrossRefPubMedPubMedCentral Holtman IR, Raj DD, Miller JA, Schaafsma W, Yin Z, Brouwer N, Wes PD, Möller T, Orre M, Kamphuis W, Hol EM, Boddeke EWGM, Eggen BJL (2015) Induction of a common microglia gene expression signature by aging and neurodegenerative conditions: a co-expression meta-analysis. Acta Neuropathol Commun 3:31. doi:10.​1186/​s40478-015-0203-5 CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Hristova M, Cuthill D, Zbarsky V, Acosta-Saltos A, Wallace A, Blight K, Buckley SMK, Peebles D, Heuer H, Waddington SN, Raivich G (2010) Activation and deactivation of periventricular white matter phagocytes during postnatal mouse development. Glia 58:11–28. doi:10.1002/glia.20896 CrossRefPubMed Hristova M, Cuthill D, Zbarsky V, Acosta-Saltos A, Wallace A, Blight K, Buckley SMK, Peebles D, Heuer H, Waddington SN, Raivich G (2010) Activation and deactivation of periventricular white matter phagocytes during postnatal mouse development. Glia 58:11–28. doi:10.​1002/​glia.​20896 CrossRefPubMed
26.
Zurück zum Zitat Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR (2000) Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20:4106–4114CrossRefPubMedPubMedCentral Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR (2000) Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20:4106–4114CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Karram K, Goebbels S, Schwab M, Jennissen K, Seifert G, Steinhäuser C, Nave K-A, Trotter J (2008) NG2-expressing cells in the nervous system revealed by the NG2-EYFP-knockin mouse. Genesis 46:743–757. doi:10.1002/dvg.20440 CrossRefPubMed Karram K, Goebbels S, Schwab M, Jennissen K, Seifert G, Steinhäuser C, Nave K-A, Trotter J (2008) NG2-expressing cells in the nervous system revealed by the NG2-EYFP-knockin mouse. Genesis 46:743–757. doi:10.​1002/​dvg.​20440 CrossRefPubMed
28.
Zurück zum Zitat Kierdorf K, Erny D, Goldmann T, Sander V, Schulz C, Perdiguero EG, Wieghofer P, Heinrich A, Riemke P, Holscher C, Muller DN, Luckow B, Brocker T, Debowski K, Fritz G, Opdenakker G, Diefenbach A, Biber K, Heikenwalder M, Geissmann F, Rosenbauer F, Prinz M (2013) Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat Neurosci 16:273–280. doi:10.1038/nn.3318 CrossRefPubMed Kierdorf K, Erny D, Goldmann T, Sander V, Schulz C, Perdiguero EG, Wieghofer P, Heinrich A, Riemke P, Holscher C, Muller DN, Luckow B, Brocker T, Debowski K, Fritz G, Opdenakker G, Diefenbach A, Biber K, Heikenwalder M, Geissmann F, Rosenbauer F, Prinz M (2013) Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat Neurosci 16:273–280. doi:10.​1038/​nn.​3318 CrossRefPubMed
30.
Zurück zum Zitat Ling EA (1979) Transformation of monocytes into amoeboid microglia in the corpus callosum of postnatal rats, as shown by labelling monocytes by carbon particles. J Anat 128:847–858PubMedPubMedCentral Ling EA (1979) Transformation of monocytes into amoeboid microglia in the corpus callosum of postnatal rats, as shown by labelling monocytes by carbon particles. J Anat 128:847–858PubMedPubMedCentral
32.
Zurück zum Zitat Matcovitch-Natan O, Winter DR, Giladi A, Vargas Aguilar S, Spinrad A, Sarrazin S, Ben-Yehuda H, David E, Zelada González F, Perrin P, Keren-Shaul H, Gury M, Lara-Astaiso D, Thaiss CA, Cohen M, Bahar Halpern K, Baruch K, Deczkowska A, Lorenzo-Vivas E, Itzkovitz S, Elinav E, Sieweke MH, Schwartz M, Amit I (2016) Microglia development follows a stepwise program to regulate brain homeostasis. Science. doi:10.1126/science.aad8670 PubMed Matcovitch-Natan O, Winter DR, Giladi A, Vargas Aguilar S, Spinrad A, Sarrazin S, Ben-Yehuda H, David E, Zelada González F, Perrin P, Keren-Shaul H, Gury M, Lara-Astaiso D, Thaiss CA, Cohen M, Bahar Halpern K, Baruch K, Deczkowska A, Lorenzo-Vivas E, Itzkovitz S, Elinav E, Sieweke MH, Schwartz M, Amit I (2016) Microglia development follows a stepwise program to regulate brain homeostasis. Science. doi:10.​1126/​science.​aad8670 PubMed
34.
Zurück zum Zitat Meuwissen MEC, Schot R, Buta S, Oudesluijs G, Tinschert S, Speer SD, Li Z, van Unen L, Heijsman D, Goldmann T, Lequin MH, Kros JM, Stam W, Hermann M, Willemsen R, Brouwer RWW, Van Ijcken WFJ, Martin-Fernandez M, de Coo I, Dudink J, de Vries FAT, Bertoli Avella A, Prinz M, Crow YJ, Verheijen FW, Pellegrini S, Bogunovic D, Mancini GMS (2016) Human USP18 deficiency underlies type 1 interferonopathy leading to severe pseudo-TORCH syndrome. J Exp Med 213:1163. doi:10.1084/jem.20151529 CrossRefPubMedPubMedCentral Meuwissen MEC, Schot R, Buta S, Oudesluijs G, Tinschert S, Speer SD, Li Z, van Unen L, Heijsman D, Goldmann T, Lequin MH, Kros JM, Stam W, Hermann M, Willemsen R, Brouwer RWW, Van Ijcken WFJ, Martin-Fernandez M, de Coo I, Dudink J, de Vries FAT, Bertoli Avella A, Prinz M, Crow YJ, Verheijen FW, Pellegrini S, Bogunovic D, Mancini GMS (2016) Human USP18 deficiency underlies type 1 interferonopathy leading to severe pseudo-TORCH syndrome. J Exp Med 213:1163. doi:10.​1084/​jem.​20151529 CrossRefPubMedPubMedCentral
35.
Zurück zum Zitat Mildner A, Mack M, Schmidt H, Brück W, Djukic M, Zabel MD, Hille A, Priller J, Prinz M (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 CrossRefPubMed Mildner A, Mack M, Schmidt H, Brück W, Djukic M, Zabel MD, Hille A, Priller J, Prinz M (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 CrossRefPubMed
36.
Zurück zum Zitat Mildner A, Schmidt H, Nitsche M, Merkler D, Hanisch U-K, Mack M, Heikenwalder M, Bruck W, Priller J, Prinz M (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 CrossRefPubMed Mildner A, Schmidt H, Nitsche M, Merkler D, Hanisch U-K, Mack M, Heikenwalder M, Bruck W, Priller J, Prinz M (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 CrossRefPubMed
37.
Zurück zum Zitat Miron VE, Boyd A, Zhao J-W, Yuen TJ, Ruckh JM, Shadrach JL, van Wijngaarden P, Wagers AJ, Williams A, Franklin RJ, ffrench-Constant C (2013) M2 microglia/macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat Neurosci 16:1211–1218. doi:10.1038/nn.3469 CrossRefPubMedPubMedCentral Miron VE, Boyd A, Zhao J-W, Yuen TJ, Ruckh JM, Shadrach JL, van Wijngaarden P, Wagers AJ, Williams A, Franklin RJ, ffrench-Constant C (2013) M2 microglia/macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat Neurosci 16:1211–1218. doi:10.​1038/​nn.​3469 CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat Molawi K, Wolf Y, Kandalla PK, Favret J, Hagemeyer N, Frenzel K, Pinto AR, Klapproth K, Henri S, Malissen B, Rodewald H-R, Rosenthal NA, Bajenoff M, Prinz M, Jung S, Sieweke MH (2014) Progressive replacement of embryo-derived cardiac macrophages with age. J Exp Med 211:2151–2158. doi:10.1084/jem.20140639 CrossRefPubMedPubMedCentral Molawi K, Wolf Y, Kandalla PK, Favret J, Hagemeyer N, Frenzel K, Pinto AR, Klapproth K, Henri S, Malissen B, Rodewald H-R, Rosenthal NA, Bajenoff M, Prinz M, Jung S, Sieweke MH (2014) Progressive replacement of embryo-derived cardiac macrophages with age. J Exp Med 211:2151–2158. doi:10.​1084/​jem.​20140639 CrossRefPubMedPubMedCentral
41.
Zurück zum Zitat Naj AC, Jun G, Beecham GW, Wang L-S, Vardarajan BN, Buros J, Gallins PJ, Buxbaum JD, Jarvik GP, Crane PK, Larson EB, Bird TD, Boeve BF, Graff-Radford NR et al (2011) Common variants at MS4A4/MS4A6E, CD2AP, CD33 and EPHA1 are associated with late-onset Alzheimer’s disease. Nat Genet 43:436–441. doi:10.1038/ng.801 CrossRefPubMedPubMedCentral Naj AC, Jun G, Beecham GW, Wang L-S, Vardarajan BN, Buros J, Gallins PJ, Buxbaum JD, Jarvik GP, Crane PK, Larson EB, Bird TD, Boeve BF, Graff-Radford NR et al (2011) Common variants at MS4A4/MS4A6E, CD2AP, CD33 and EPHA1 are associated with late-onset Alzheimer’s disease. Nat Genet 43:436–441. doi:10.​1038/​ng.​801 CrossRefPubMedPubMedCentral
42.
44.
Zurück zum Zitat Paloneva J, Manninen T, Christman G, Hovanes K, Mandelin J, Adolfsson R, Bianchin M, Bird T, Miranda R, Salmaggi A, Tranebjærg L, Konttinen Y, Peltonen L (2002) Mutations in two genes encoding different subunits of a receptor signaling complex result in an identical disease phenotype. Am J Hum Genet 71:656–662. doi:10.1086/342259 CrossRefPubMedPubMedCentral Paloneva J, Manninen T, Christman G, Hovanes K, Mandelin J, Adolfsson R, Bianchin M, Bird T, Miranda R, Salmaggi A, Tranebjærg L, Konttinen Y, Peltonen L (2002) Mutations in two genes encoding different subunits of a receptor signaling complex result in an identical disease phenotype. Am J Hum Genet 71:656–662. doi:10.​1086/​342259 CrossRefPubMedPubMedCentral
45.
Zurück zum Zitat Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, Ragozzino D, Gross CT (2011) Synaptic pruning by microglia is necessary for normal brain development. Science 333:1456–1458. doi:10.1126/science.1202529 CrossRefPubMed Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, Ragozzino D, Gross CT (2011) Synaptic pruning by microglia is necessary for normal brain development. Science 333:1456–1458. doi:10.​1126/​science.​1202529 CrossRefPubMed
49.
Zurück zum Zitat Poggi G, Boretius S, Möbius W, Moschny N, Baudewig J, Ruhwedel T, Hassouna I, Wieser GL, Werner HB, Goebbels S, Nave K, Ehrenreich H (2016) Cortical network dysfunction caused by a subtle defect of myelination. Glia 64:2025–2040. doi:10.1002/glia.23039 CrossRefPubMedPubMedCentral Poggi G, Boretius S, Möbius W, Moschny N, Baudewig J, Ruhwedel T, Hassouna I, Wieser GL, Werner HB, Goebbels S, Nave K, Ehrenreich H (2016) Cortical network dysfunction caused by a subtle defect of myelination. Glia 64:2025–2040. doi:10.​1002/​glia.​23039 CrossRefPubMedPubMedCentral
51.
Zurück zum Zitat Prinz M, Erny D, Hagemeyer N (2017) Ontogeny and homeostasis of CNS myeloid cells. Nat Immunol 18:385CrossRefPubMed Prinz M, Erny D, Hagemeyer N (2017) Ontogeny and homeostasis of CNS myeloid cells. Nat Immunol 18:385CrossRefPubMed
52.
53.
Zurück zum Zitat Prinz M, Priller J (2017) The role of peripheral immune cells in the CNS in steady state and disease. Nat Neurosci 20:136–144CrossRefPubMed Prinz M, Priller J (2017) The role of peripheral immune cells in the CNS in steady state and disease. Nat Neurosci 20:136–144CrossRefPubMed
54.
Zurück zum Zitat R Core Team R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna R Core Team R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
55.
Zurück zum Zitat Rademakers R, Baker M, Nicholson AM, Rutherford NJ, Finch N, Soto-Ortolaza A, Lash J, Wider C, Wojtas A, DeJesus-Hernandez M, Adamson J, Kouri N, Sundal C, Shuster EA, Aasly J, MacKenzie J, Roeber S, Kretzschmar HA, Boeve BF, Knopman DS, Petersen RC, Cairns NJ, Ghetti B, Spina S, Garbern J, Tselis AC, Uitti R, Das P, Van Gerpen JA, Meschia JF, Levy S, Broderick DF, Graff-Radford N, Ross OA, Miller BB, Swerdlow RH, Dickson DW, Wszolek ZK (2012) Mutations in the colony stimulating factor 1 receptor (CSF1R) gene cause hereditary diffuse leukoencephalopathy with spheroids. Nat Genet 44:200–205. doi:10.1038/ng.1027 CrossRef Rademakers R, Baker M, Nicholson AM, Rutherford NJ, Finch N, Soto-Ortolaza A, Lash J, Wider C, Wojtas A, DeJesus-Hernandez M, Adamson J, Kouri N, Sundal C, Shuster EA, Aasly J, MacKenzie J, Roeber S, Kretzschmar HA, Boeve BF, Knopman DS, Petersen RC, Cairns NJ, Ghetti B, Spina S, Garbern J, Tselis AC, Uitti R, Das P, Van Gerpen JA, Meschia JF, Levy S, Broderick DF, Graff-Radford N, Ross OA, Miller BB, Swerdlow RH, Dickson DW, Wszolek ZK (2012) Mutations in the colony stimulating factor 1 receptor (CSF1R) gene cause hereditary diffuse leukoencephalopathy with spheroids. Nat Genet 44:200–205. doi:10.​1038/​ng.​1027 CrossRef
58.
Zurück zum Zitat Rio-Hortega P (1932) Microglia. Cytol Cell Pathol Nerv Syst 2:482–534 Rio-Hortega P (1932) Microglia. Cytol Cell Pathol Nerv Syst 2:482–534
61.
Zurück zum Zitat Safaiyan S, Kannaiyan N, Snaidero N, Brioschi S, Biber K, Yona S, Edinger AL, Jung S, Rossner MJ, Simons M (2016) Age-related myelin degradation burdens the clearance function of microglia during aging. Nat Neurosci 19:995–998CrossRefPubMed Safaiyan S, Kannaiyan N, Snaidero N, Brioschi S, Biber K, Yona S, Edinger AL, Jung S, Rossner MJ, Simons M (2016) Age-related myelin degradation burdens the clearance function of microglia during aging. Nat Neurosci 19:995–998CrossRefPubMed
63.
Zurück zum Zitat Scheffel J, Regen T, Van Rossum D, Seifert S, Ribes S, Nau R, Parsa R, Harris RA, Boddeke HWGM, Chuang H-N, Pukrop T, Wessels JT, Jürgens T, Merkler D, Brück W, Schnaars M, Simons M, Kettenmann H, Hanisch U-K (2012) Toll-like receptor activation reveals developmental reorganization and unmasks responder subsets of microglia. Glia 60:1930–1943. doi:10.1002/glia.22409 CrossRefPubMed Scheffel J, Regen T, Van Rossum D, Seifert S, Ribes S, Nau R, Parsa R, Harris RA, Boddeke HWGM, Chuang H-N, Pukrop T, Wessels JT, Jürgens T, Merkler D, Brück W, Schnaars M, Simons M, Kettenmann H, Hanisch U-K (2012) Toll-like receptor activation reveals developmental reorganization and unmasks responder subsets of microglia. Glia 60:1930–1943. doi:10.​1002/​glia.​22409 CrossRefPubMed
64.
Zurück zum Zitat Schulz C, Perdiguero EG, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SEW, Pollard JW, Frampton J, Liu KJ, Geissmann F (2012) A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336:86–90. doi:10.1126/science.1219179 CrossRefPubMed Schulz C, Perdiguero EG, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SEW, Pollard JW, Frampton J, Liu KJ, Geissmann F (2012) A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336:86–90. doi:10.​1126/​science.​1219179 CrossRefPubMed
68.
Zurück zum Zitat Skripuletz T, Miller E, Moharregh-Khiabani D, Blank A, Pul R, Gudi V, Trebst C, Stangel M (2010) Beneficial effects of minocycline on cuprizone induced cortical demyelination. Neurochem Res 35:1422–1433. doi:10.1007/s11064-010-0202-7 CrossRefPubMed Skripuletz T, Miller E, Moharregh-Khiabani D, Blank A, Pul R, Gudi V, Trebst C, Stangel M (2010) Beneficial effects of minocycline on cuprizone induced cortical demyelination. Neurochem Res 35:1422–1433. doi:10.​1007/​s11064-010-0202-7 CrossRefPubMed
70.
Zurück zum Zitat Ueno M, Fujita Y, Tanaka T, Nakamura Y, Kikuta J, Ishii M, Yamashita T (2013) Layer V cortical neurons require microglial support for survival during postnatal development. Nat Neurosci 16:543–551. doi:10.1038/nn.3358 CrossRefPubMed Ueno M, Fujita Y, Tanaka T, Nakamura Y, Kikuta J, Ishii M, Yamashita T (2013) Layer V cortical neurons require microglial support for survival during postnatal development. Nat Neurosci 16:543–551. doi:10.​1038/​nn.​3358 CrossRefPubMed
71.
Zurück zum Zitat Viganò F, Schneider S, Cimino M, Bonfanti E, Gelosa P, Sironi L, Abbracchio MP, Dimou L (2016) GPR17 expressing NG2-Glia: oligodendrocyte progenitors serving as a reserve pool after injury. Glia 64:287–299. doi:10.1002/glia.22929 CrossRefPubMed Viganò F, Schneider S, Cimino M, Bonfanti E, Gelosa P, Sironi L, Abbracchio MP, Dimou L (2016) GPR17 expressing NG2-Glia: oligodendrocyte progenitors serving as a reserve pool after injury. Glia 64:287–299. doi:10.​1002/​glia.​22929 CrossRefPubMed
73.
Zurück zum Zitat Ward JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 69:236–244CrossRef Ward JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 69:236–244CrossRef
74.
Zurück zum Zitat Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B (2016) gplots: various R programming tools for plotting data. R package version 3.0.1 Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B (2016) gplots: various R programming tools for plotting data. R package version 3.0.1
75.
Zurück zum Zitat Zeger M, Popken G, Zhang J, Xuan S, Lu QR, Schwab MH, Nave K-A, Rowitch D, D’Ercole AJ, Ye P (2007) Insulin-like growth factor type 1 receptor signaling in the cells of oligodendrocyte lineage is required for normal in vivo oligodendrocyte development and myelination. Glia 55:400–411. doi:10.1002/glia.20469 CrossRefPubMedPubMedCentral Zeger M, Popken G, Zhang J, Xuan S, Lu QR, Schwab MH, Nave K-A, Rowitch D, D’Ercole AJ, Ye P (2007) Insulin-like growth factor type 1 receptor signaling in the cells of oligodendrocyte lineage is required for normal in vivo oligodendrocyte development and myelination. Glia 55:400–411. doi:10.​1002/​glia.​20469 CrossRefPubMedPubMedCentral
Metadaten
Titel
Microglia contribute to normal myelinogenesis and to oligodendrocyte progenitor maintenance during adulthood
verfasst von
Nora Hagemeyer
Klara-Maria Hanft
Maria-Anna Akriditou
Nicole Unger
Eun S. Park
E. Richard Stanley
Ori Staszewski
Leda Dimou
Marco Prinz
Publikationsdatum
06.07.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
Acta Neuropathologica / Ausgabe 3/2017
Print ISSN: 0001-6322
Elektronische ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-017-1747-1

Weitere Artikel der Ausgabe 3/2017

Acta Neuropathologica 3/2017 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.