May 23, 2024
Microglia-mediated T cell infiltration drives neurodegeneration in tauopathy – Nature

Microglia-mediated T cell infiltration drives neurodegeneration in tauopathy – Nature

  • Duyckaerts, C., Delatour, B. & Potier, M. C. Classification and basic pathology of Alzheimer disease. Acta Neuropathol. 118, 5–36 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Masters, C. L. et al. Alzheimer’s disease. Nat. Rev. Dis. Primers 1, 15056 (2015).

    Article 
    PubMed 

    Google Scholar
     

  • Jack, C. R. Jr & Holtzman, D. M. Biomarker modeling of Alzheimer’s disease. Neuron 80, 1347–1358 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Musiek, E. S. & Holtzman, D. M. Three dimensions of the amyloid hypothesis: time, space and ‘wingmen’. Nat. Neurosci. 18, 800–806 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Giannakopoulos, P. et al. Tangle and neuron numbers, but not amyloid load, predict cognitive status in Alzheimer’s disease. Neurology 60, 1495–1500 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen, X. & Holtzman, D. M. Emerging roles of innate and adaptive immunity in Alzheimer’s disease. Immunity 55, 2236–2254 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ulrich, J. D. et al. Altered microglial response to Aβ plaques in APPPS1-21 mice heterozygous for TREM2. Mol. Neurodegener. 9, 20 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xiong, M. et al. APOE immunotherapy reduces cerebral amyloid angiopathy and amyloid plaques while improving cerebrovascular function. Sci. Transl. Med. 13, eabd7522 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rupp, N. J., Wegenast-Braun, B. M., Radde, R., Calhoun, M. E. & Jucker, M. Early onset amyloid lesions lead to severe neuritic abnormalities and local, but not global neuron loss in APPPS1 transgenic mice. Neurobiol. Aging 32, 2324 (2011).

    Article 

    Google Scholar
     

  • Giannoni, P. et al. Cerebrovascular pathology during the progression of experimental Alzheimer’s disease. Neurobiol. Dis. 88, 107–117 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yoshiyama, Y. et al. Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 53, 337–351 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Long, J. M. & Holtzman, D. M. Alzheimer disease: an update on pathobiology and treatment strategies. Cell 179, 312–339 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hammond, T. R., Marsh, S. E. & Stevens, B. Immune signaling in neurodegeneration. Immunity 50, 955–974 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Heneka, M. T., Kummer, M. P. & Latz, E. Innate immune activation in neurodegenerative disease. Nat. Rev. Immunol. 14, 463–477 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Krasemann, S. et al. The TREM2-APOE pathway drives the transcriptional phenotype of dysfunctional microglia in neurodegenerative diseases. Immunity 47, 566–581 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mrdjen, D. et al. High-dimensional single-cell mapping of central nervous system immune cells reveals distinct myeloid subsets in health, aging, and disease. Immunity 48, 380–395 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Prinz, M., Priller, J., Sisodia, S. S. & Ransohoff, R. M. Heterogeneity of CNS myeloid cells and their roles in neurodegeneration. Nat. Neurosci. 14, 1227–1235 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fischer, H. G. & Reichmann, G. Brain dendritic cells and macrophages/microglia in central nervous system inflammation. J. Immunol. 166, 2717–2726 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gate, D. et al. CD4+ T cells contribute to neurodegeneration in Lewy body dementia. Science 374, 868–874 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zenaro, E. et al. Neutrophils promote Alzheimer’s disease-like pathology and cognitive decline via LFA-1 integrin. Nat. Med. 21, 880–886 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Subbarayan, M. S., Hudson, C., Moss, L. D., Nash, K. R. & Bickford, P. C. T cell infiltration and upregulation of MHCII in microglia leads to accelerated neuronal loss in an alpha-synuclein rat model of Parkinson’s disease. J. Neuroinflammation 17, 242 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Garber, C. et al. T cells promote microglia-mediated synaptic elimination and cognitive dysfunction during recovery from neuropathogenic flaviviruses. Nat. Neurosci. 22, 1276–1288 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gate, D. et al. Clonally expanded CD8 T cells patrol the cerebrospinal fluid in Alzheimer’s disease. Nature 577, 399–404 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Merlini, M., Kirabali, T., Kulic, L., Nitsch, R. M. & Ferretti, M. T. Extravascular CD3+ T cells in brains of Alzheimer disease patients correlate with Tau but not with amyloid pathology: an immunohistochemical study. Neurodegener. Dis. 18, 49–56 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Laurent, C. et al. Hippocampal T cell infiltration promotes neuroinflammation and cognitive decline in a mouse model of tauopathy. Brain 140, 184–200 (2017).

    Article 
    PubMed 

    Google Scholar
     

  • Lee, S. H. et al. TREM2-independent oligodendrocyte, astrocyte, and T cell responses to tau and amyloid pathology in mouse models of Alzheimer disease. Cell Rep. 37, 110158 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Norris, G. T. & Kipnis, J. Immune cells and CNS physiology: microglia and beyond. J. Exp. Med. 216, 60–70 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen, X. et al. Transcriptomic mapping uncovers Purkinje neuron plasticity driving learning. Nature 605, 722–727 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Da Mesquita, S., Fu, Z. & Kipnis, J. The meningeal lymphatic system: a new player in neurophysiology. Neuron 100, 375–388 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Da Mesquita, S. et al. Meningeal lymphatics affect microglia responses and anti-Aβ immunotherapy. Nature 593, 255–260 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rustenhoven, J. & Kipnis, J. Bypassing the blood-brain barrier. Science 366, 1448–1449 (2019).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Rustenhoven, J. et al. Functional characterization of the dural sinuses as a neuroimmune interface. Cell 184, 1000–1016 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Korn, T. & Kallies, A. T cell responses in the central nervous system. Nat. Rev. Immunol. 17, 179–194 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Siller-Farfan, J. A. & Dushek, O. Molecular mechanisms of T cell sensitivity to antigen. Immunol. Rev. 285, 194–205 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Loetscher, M. et al. Chemokine receptor specific for IP10 and mig: structure, function, and expression in activated T-lymphocytes. J. Exp. Med. 184, 963–969 (1996).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Madore, C., Yin, Z., Leibowitz, J. & Butovsky, O. Microglia, lifestyle stress, and neurodegeneration. Immunity 52, 222–240 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gratuze, M. et al. Impact of TREM2R47H variant on tau pathology-induced gliosis and neurodegeneration. J. Clin. Invest. 130, 4954–4968 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Huang, Y. et al. Microglia use TAM receptors to detect and engulf amyloid beta plaques. Nat. Immunol. 22, 586–594 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Neefjes, J., Jongsma, M. L., Paul, P. & Bakke, O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat. Rev. Immunol. 11, 823–836 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Keren-Shaul, H. et al. A unique microglia type associated with restricting development of Alzheimer’s disease. Cell 169, 1276–1290 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mathys, H. et al. Temporal tracking of microglia activation in neurodegeneration at single-cell resolution. Cell Rep. 21, 366–380 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Filiano, A. J. et al. Unexpected role of interferon-gamma in regulating neuronal connectivity and social behaviour. Nature 535, 425–429 (2016).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Khalil, M. et al. Neurofilaments as biomarkers in neurological disorders. Nat. Rev. Neurol. 14, 577–589 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pardoll, D. M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 12, 252–264 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sharpe, A. H. & Pauken, K. E. The diverse functions of the PD1 inhibitory pathway. Nat. Rev. Immunol. 18, 153–167 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rosenzweig, N. et al. PD-1/PD-L1 checkpoint blockade harnesses monocyte-derived macrophages to combat cognitive impairment in a tauopathy mouse model. Nat. Commun. 10, 465 (2019).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Baruch, K. et al. PD-1 immune checkpoint blockade reduces pathology and improves memory in mouse models of Alzheimer’s disease. Nat. Med. 22, 135–137 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kumagai, S. et al. The PD-1 expression balance between effector and regulatory T cells predicts the clinical efficacy of PD-1 blockade therapies. Nat. Immunol. 21, 1346–1358 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Turley, S. J., Fletcher, A. L. & Elpek, K. G. The stromal and haematopoietic antigen-presenting cells that reside in secondary lymphoid organs. Nat. Rev. Immunol. 10, 813–825 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kigerl, K. A., de Rivero Vaccari, J. P., Dietrich, W. D., Popovich, P. G. & Keane, R. W. Pattern recognition receptors and central nervous system repair. Exp. Neurol. 258, 5–16 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Huynh, T. V. et al. Lack of hepatic apoE does not influence early Aβ deposition: observations from a new APOE knock-in model. Mol. Neurodegener. 14, 37 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Noguchi, T. et al. Temporally distinct PD-L1 expression by tumor and host cells contributes to immune escape. Cancer Immunol. Res. 5, 106–117 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wozniak, D. F. et al. Motivational disturbances and effects of L-dopa administration in neurofibromatosis-1 model mice. PLoS ONE 8, e66024 (2013).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yuede, C. M. et al. Behavioral consequences of NMDA antagonist-induced neuroapoptosis in the infant mouse brain. PLoS ONE 5, e11374 (2010).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Khuchua, Z. et al. Deletion of the N-terminus of murine map2 by gene targeting disrupts hippocampal ca1 neuron architecture and alters contextual memory. Neuroscience 119, 101–111 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hammond, T. R. et al. Single-cell RNA sequencing of microglia throughout the mouse lifespan and in the injured brain reveals complex cell-state changes. Immunity 50, 253–271 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Source link