154
Views
8
CrossRef citations to date
0
Altmetric
Original Research

Microglia Impede Oligodendrocyte Generation in Aged Brain

, , , , , , & show all
Pages 6813-6831 | Published online: 11 Dec 2021

References

  • Pini L, Pievani M, Bocchetta M, et al. Brain atrophy in Alzheimer’s Disease and aging. Ageing Res Rev. 2016;30:25–48. doi:10.1016/j.arr.2016.01.002
  • Mayne K, White JA, McMurran CE, Rivera FJ, de la Fuente AG. Aging and neurodegenerative disease: is the adaptive immune system a friend or foe? Front Aging Neurosci. 2020;12:572090. doi:10.3389/fnagi.2020.572090
  • Li C, Zhang L, Chao F, Xiao Q, Luo Y, Tang Y. Stereological quantification of age-related changes in myelinated fibers of rat white matter. Neuroreport. 2017;28(1):42–49. doi:10.1097/WNR.0000000000000706
  • Guttmann CR, Jolesz FA, Kikinis R, et al. White matter changes with normal aging. Neurology. 1998;50(4):972–978. doi:10.1212/wnl.50.4.972
  • Stangel M, Kuhlmann T, Matthews PM, Kilpatrick TJ. Achievements and obstacles of remyelinating therapies in multiple sclerosis. Nat Rev Neurol. 2017;13(12):742–754. doi:10.1038/nrneurol.2017.139
  • Ruckh JM, Zhao JW, Shadrach JL, et al. Rejuvenation of regeneration in the aging central nervous system. Cell Stem Cell. 2012;10(1):96–103. doi:10.1016/j.stem.2011.11.019
  • Niraula A, Sheridan JF, Godbout JP. Microglia priming with aging and stress. Neuropsychopharmacology. 2017;42(1):318–333. doi:10.1038/npp.2016.185
  • Pang Y, Campbell L, Zheng B, Fan L, Cai Z, Rhodes P. Lipopolysaccharide-activated microglia induce death of oligodendrocyte progenitor cells and impede their development. Neuroscience. 2010;166(2):464–475. doi:10.1016/j.neuroscience.2009.12.040
  • Taylor DL, Pirianov G, Holland Set al. Attenuation of proliferation in oligodendrocyte precursor cells by activated microglia. J Neurosci Res. 2010;88(8):1632–1644. doi:10.1002/jnr.22335.
  • Yeo YA, Martinez Gomez JM, Croxford JL, Gasser S, Ling EA, Schwarz H. CD137 ligand activated microglia induces oligodendrocyte apoptosis via reactive oxygen species. J Neuroinflammation. 2012;9:173. doi:10.1186/1742-2094-9-173
  • Voss EV, Skuljec J, Gudi V, et al. Characterisation of microglia during de- and remyelination: can they create a repair promoting environment? Neurobiol Dis. 2012;45(1):519–528. doi:10.1016/j.nbd.2011.09.008
  • Nicholas RS, Stevens S, Wing MG, Compston DA. Microglia-derived IGF-2 prevents TNFalpha induced death of mature oligodendrocytes in vitro. J Neuroimmunol. 2002;124(1–2):36–44. doi:10.1016/s0165-5728(02)00011-5
  • Pasquini LA, Millet V, Hoyos HC, et al. Galectin-3 drives oligodendrocyte differentiation to control myelin integrity and function. Cell Death Differ. 2011;18(11):1746–1756. doi:10.1038/cdd.2011.40
  • Miron VE, Boyd A, Zhao JW, et al. M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat Neurosci. 2013;16(9):1211–1218. doi:10.1038/nn.3469
  • Mason JL, Suzuki K, Chaplin DD, Matsushima GK. Interleukin-1beta promotes repair of the CNS. J Neurosci. 2001;21(18):7046–7052. doi:10.1523/JNEUROSCI.21-18-07046.2001
  • Neumann H, Kotter MR, Franklin RJ. Debris clearance by microglia: an essential link between degeneration and regeneration. Brain. 2009;132(Pt 2):288–295. doi:10.1093/brain/awn109
  • Marques S, Zeisel A, Codeluppi S, et al. Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system. Science. 2016;352(6291):1326–1329. doi:10.1126/science.aaf6463
  • Jin C, Shao Y, Zhang X, et al. A unique type of highly-activated microglia evoking brain inflammation via Mif/Cd74 signaling axis in aged mice. Agingdis. doi:10.14336/ad.2021.0520
  • Yeh FC, Verstynen TD, Wang Y, Fernandez-Miranda JC, Tseng WY. Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS One. 2013;8(11):e80713. doi:10.1371/journal.pone.0080713
  • Wang F, Ren SY, Chen JF, et al. Myelin degeneration and diminished myelin renewal contribute to age-related deficits in memory. Nat Neurosci. 2020;23(4):481–486. doi:10.1038/s41593-020-0588-8
  • Stuart T, Butler A, Hoffman P, et al. Comprehensive integration of single-cell data. Cell. 2019;177(7):1888–1902 e21. doi:10.1016/j.cell.2019.05.031
  • Finak G, McDavid A, Yajima M, et al. MAST: a flexible statistical framework for assessing transcriptional changes and characterizing heterogeneity in single-cell RNA sequencing data. Genome Biol. 2015;16:278. doi:10.1186/s13059-015-0844-5
  • Zhou Y, Zhou B, Pache L, et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun. 2019;10(1):1523. doi:10.1038/s41467-019-09234-6
  • Walter W, Sanchez-Cabo F, Ricote M. GOplot: an R package for visually combining expression data with functional analysis. Bioinformatics. 2015;31(17):2912–2914. doi:10.1093/bioinformatics/btv300
  • Trapnell C, Cacchiarelli D, Grimsby J, et al. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat Biotechnol. 2014;32(4):381–386. doi:10.1038/nbt.2859
  • Qiu X, Mao Q, Tang Y, et al. Reversed graph embedding resolves complex single-cell trajectories. Nat Methods. 2017;14(10):979–982. doi:10.1038/nmeth.4402
  • Qiu X, Hill A, Packer J, Lin D, Ma YA, Trapnell C. Single-cell mRNA quantification and differential analysis with Census. Nat Methods. 2017;14(3):309–315. doi:10.1038/nmeth.4150
  • Han H, Cho JW, Lee S, et al. TRRUST v2: an expanded reference database of human and mouse transcriptional regulatory interactions. Nucleic Acids Res. 2018;46(D1):D380–D386. doi:10.1093/nar/gkx1013
  • Safaiyan S, Besson-Girard S, Kaya T, et al. White matter aging drives microglial diversity. Neuron. 2021;109(7):1100–1117 e10. doi:10.1016/j.neuron.2021.01.027
  • Aibar S, Gonzalez-Blas CB, Moerman T, et al. SCENIC: single-cell regulatory network inference and clustering. Nat Methods. 2017;14(11):1083–1086. doi:10.1038/nmeth.4463
  • Sullivan EV, Rohlfing T, Pfefferbaum A. Longitudinal study of callosal microstructure in the normal adult aging brain using quantitative DTI fiber tracking. Dev Neuropsychol. 2010;35(3):233–256. doi:10.1080/87565641003689556
  • Kim JB, Lee H, Arauzo-Bravo MJ, et al. Oct4-induced oligodendrocyte progenitor cells enhance functional recovery in spinal cord injury model. EMBO J. 2015;34(23):2971–2983. doi:10.15252/embj.201592652
  • Dugas JC, Tai YC, Speed TP, Ngai J, Barres BA. Functional genomic analysis of oligodendrocyte differentiation. J Neurosci. 2006;26(43):10967–10983. doi:10.1523/JNEUROSCI.2572-06.2006
  • Bercury KK, Macklin WB. Dynamics and mechanisms of CNS myelination. Dev Cell. 2015;32(4):447–458. doi:10.1016/j.devcel.2015.01.016
  • Voskuhl RR, Itoh N, Tassoni A, et al. Gene expression in oligodendrocytes during remyelination reveals cholesterol homeostasis as a therapeutic target in multiple sclerosis. Proc Natl Acad Sci U S A. 2019;116(20):10130–10139. doi:10.1073/pnas.1821306116
  • Marcus J, Popko B. Galactolipids are molecular determinants of myelin development and axo-glial organization. Biochim Biophys Acta. 2002;1573(3):406–413. doi:10.1016/s0304-4165(02)00410-5
  • Lloyd AF, Miron VE. The pro-remyelination properties of microglia in the central nervous system. Nat Rev Neurol. 2019;15(8):447–458. doi:10.1038/s41582-019-0184-2
  • Olah M, Amor S, Brouwer N, et al. Identification of a microglia phenotype supportive of remyelination. Glia. 2012;60(2):306–321. doi:10.1002/glia.21266
  • Ma J, Tanaka KF, Shimizu T, et al. Microglial cystatin F expression is a sensitive indicator for ongoing demyelination with concurrent remyelination. J Neurosci Res. 2011;89(5):639–649. doi:10.1002/jnr.22567
  • Spaas J, van Veggel L, Schepers M, et al. Oxidative stress and impaired oligodendrocyte precursor cell differentiation in neurological disorders. Cell Mol Life Sci. 2021;78(10):4615–4637. doi:10.1007/s00018-021-03802-0
  • Auderset L, Pitman KA, Cullen CL, et al. Low-density lipoprotein Receptor-Related Protein 1 (LRP1) is a negative regulator of oligodendrocyte progenitor cell differentiation in the adult mouse brain. Original research. Front Cell Devel Biol. 2020;8:1067. doi:10.3389/fcell.2020.564351
  • Zhu Q, Zhao X, Zheng K, et al. Genetic evidence that Nkx2.2 and Pdgfra are major determinants of the timing of oligodendrocyte differentiation in the developing CNS. Development. 2014;141(3):548–555. doi:10.1242/dev.095323
  • Yang HJ, Vainshtein A, Maik-Rachline G, Peles E. G protein-coupled receptor 37 is a negative regulator of oligodendrocyte differentiation and myelination. Nat Commun. 2016;7:10884. doi:10.1038/ncomms10884
  • Wang W, Zhao F, Ma X, Perry G, Zhu X. Mitochondria dysfunction in the pathogenesis of Alzheimer’s disease: recent advances. Mol Neurodegener. 2020;15(1):30. doi:10.1186/s13024-020-00376-6
  • Pohlkamp T, Wasser CR, Herz J. Functional roles of the interaction of APP and lipoprotein receptors. Front Mol Neurosci. 2017;10:54. doi:10.3389/fnmol.2017.00054
  • Spuch C, Ortolano S, Navarro C. New insights in the amyloid-Beta interaction with mitochondria. J Aging Res. 2012;2012:324968. doi:10.1155/2012/324968
  • Kanekiyo T, Bu G. The low-density lipoprotein receptor-related protein 1 and amyloid-beta clearance in Alzheimer’s disease. Front Aging Neurosci. 2014;6:93. doi:10.3389/fnagi.2014.00093
  • Fang N, Cheng J, Zhang C, et al. Sirt2 epigenetically down-regulates PDGFRalpha expression and promotes CG4 cell differentiation. Cell Cycle. 2019;18(10):1095–1109. doi:10.1080/15384101.2019.1609818
  • Kotter MR, Stadelmann C, Hartung HP. Enhancing remyelination in disease–can we wrap it up? Brain. 2011;134(Pt 7)):1882–1900. doi:10.1093/brain/awr014
  • Renault MA, Jalvy S, Belloc I, et al. AP-1 is involved in UTP-induced osteopontin expression in arterial smooth muscle cells. Circ Res. 2003;93(7):674–681. doi:10.1161/01.RES.0000094747.05021.62
  • Gafencu AV, Robciuc MR, Fuior E, Zannis VI, Kardassis D, Simionescu M. Inflammatory signaling pathways regulating ApoE gene expression in macrophages. J Biol Chem. 2007;282(30):21776–21785. doi:10.1074/jbc.M611422200
  • Wai PY, Mi Z, Gao C, Guo H, Marroquin C, Kuo PC. Ets-1 and runx2 regulate transcription of a metastatic gene, osteopontin, in murine colorectal cancer cells. J Biol Chem. 2006;281(28):18973–18982. doi:10.1074/jbc.M511962200
  • Stock M, Schafer H, Stricker S, Gross G, Mundlos S, Otto F. Expression of galectin-3 in skeletal tissues is controlled by Runx2. J Biol Chem. 2003;278(19):17360–17367. doi:10.1074/jbc.M207631200
  • Kim S, Koga T, Isobe M, et al. Stat1 functions as a cytoplasmic attenuator of Runx2 in the transcriptional program of osteoblast differentiation. Genes Dev. 2003;17(16):1979–1991. doi:10.1101/gad.1119303
  • Trusca VG, Fuior EV, Florea IC, Kardassis D, Simionescu M, Gafencu AV. Macrophage-specific up-regulation of apolipoprotein E gene expression by STAT1 is achieved via long range genomic interactions. J Biol Chem. 2011;286(16):13891–13904. doi:10.1074/jbc.M110.179572
  • Wynes MW, Riches DW. Induction of macrophage insulin-like growth factor-I expression by the Th2 cytokines IL-4 and IL-13. J Immunol. 2003;171(7):3550–3559. doi:10.4049/jimmunol.171.7.3550
  • Hogan JC, Stephens JM. STAT 1 binds to the LPL promoter in vitro. Biochem Biophys Res Commun. 2003;307(2):350–354. doi:10.1016/s0006-291x(03)01198-7
  • Murakami K, Jiang YP, Tanaka T, Bando Y, Mitrovic B, Yoshida S. In vivo analysis of kallikrein-related peptidase 6 (KLK6) function in oligodendrocyte development and the expression of myelin proteins. Neuroscience. 2013;236:1–11. doi:10.1016/j.neuroscience.2012.12.073
  • Bando Y, Hagiwara Y, Suzuki Y, et al. Kallikrein 6 secreted by oligodendrocytes regulates the progression of experimental autoimmune encephalomyelitis. Glia. 2018;66(2):359–378. doi:10.1002/glia.23249
  • Duncan ID, Radcliff AB, Heidari M, Kidd G, August BK, Wierenga LA. The adult oligodendrocyte can participate in remyelination. Proc Natl Acad Sci U S A. 2018;115(50):E11807–E11816. doi:10.1073/pnas.1808064115
  • Floriddia EM, Lourenço T, Zhang S, et al. Distinct oligodendrocyte populations have spatial preference and different responses to spinal cord injury. Nat Commun. 2020;11(1):5860. doi:10.1038/s41467-020-19453-x
  • Hughes EG, Orthmann-Murphy JL, Langseth AJ, Bergles DE. Myelin remodeling through experience-dependent oligodendrogenesis in the adult somatosensory cortex. Nat Neurosci. 2018;21(5):696–706. doi:10.1038/s41593-018-0121-5
  • Chacon-de-la-rocha I, Fryatt G, Rivera AD, et al. Accelerated dystrophy and decay of oligodendrocyte precursor cells in the APP/PS1 model of Alzheimer’s-like pathology. Front Cell Neurosci. 2020;14:575082. doi:10.3389/fncel.2020.575082
  • Young KM, Psachoulia K, Tripathi RB, et al. Oligodendrocyte dynamics in the healthy adult CNS: evidence for myelin remodeling. Neuron. 2013;77(5):873–885. doi:10.1016/j.neuron.2013.01.006
  • Levine JM, Reynolds R. Activation and proliferation of endogenous oligodendrocyte precursor cells during ethidium bromide-induced demyelination. Exp Neurol. 1999;160(2):333–347. doi:10.1006/exnr.1999.7224
  • Hughes EG, Kang SH, Fukaya M, Bergles DE. Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat Neurosci. 2013;16(6):668–676. doi:10.1038/nn.3390
  • Rosko L, Smith VN, Yamazaki R, Huang JK. Oligodendrocyte bioenergetics in health and disease. Neuroscientist. 2019;25(4):334–343. doi:10.1177/1073858418793077
  • Lopez-Otin C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell. 2013;153(6):1194–1217. doi:10.1016/j.cell.2013.05.039
  • Neumann B, Segel M, Chalut KJ, Franklin RJ. Remyelination and ageing: reversing the ravages of time. Mult Scler. 2019;25(14):1835–1841. doi:10.1177/1352458519884006
  • Wang J-B, Zhang Z, Li J-N, et al. SPP1 promotes Schwann cell proliferation and survival through PKCα by binding with CD44 and αvβ3 after peripheral nerve injury. Cell Biosci. 2020;10(1):98. doi:10.1186/s13578-020-00458-4
  • Selvaraju R, Bernasconi L, Losberger C, et al. Osteopontin is upregulated during in vivo demyelination and remyelination and enhances myelin formation in vitro. Mol Cell Neurosci. 2004;25(4):707–721. doi:10.1016/j.mcn.2003.12.014
  • Carlo AS. Sortilin, a novel APOE receptor implicated in Alzheimer disease. Prion. 2013;7(5):378–382. doi:10.4161/pri.26746
  • Chen GF, Xu TH, Yan Y, et al. Amyloid beta: structure, biology and structure-based therapeutic development. Acta Pharmacol Sin. 2017;38(9):1205–1235. doi:10.1038/aps.2017.28
  • Vanzulli I, Papanikolaou M, De-la-rocha IC, et al. Disruption of oligodendrocyte progenitor cells is an early sign of pathology in the triple transgenic mouse model of Alzheimer’s disease. Neurobiol Aging. 2020;94:130–139. doi:10.1016/j.neurobiolaging.2020.05.016
  • Li W, Tang Y, Fan Z, et al. Autophagy is involved in oligodendroglial precursor-mediated clearance of amyloid peptide. Mol Neurodegener. 2013;8:27. doi:10.1186/1750-1326-8-27
  • Boriero D, Carcereri de Prati A, Antonini L, et al. The anti-STAT1 polyphenol myricetin inhibits M1 microglia activation and counteracts neuronal death. FEBS J. 2021;288(7):2347–2359. doi:10.1111/febs.15577
  • Hsu WL, Ma YL, Hsieh DY, Liu YC, Lee EH. STAT1 negatively regulates spatial memory formation and mediates the memory-impairing effect of Abeta. Neuropsychopharmacology. 2014;39(3):746–758. doi:10.1038/npp.2013.263
  • Lin W, Lin Y. Interferon-gamma inhibits central nervous system myelination through both STAT1-dependent and STAT1-independent pathways. J Neurosci Res. 2010;88(12):2569–2577. doi:10.1002/jnr.22425