Cited by 16Alzheimer's disease research and treatmentsNeuroscience and Neuropharmacology ResearchNeural dynamics and brain function

Selective dysfunction of fast-spiking inhibitory interneurons and disruption of perineuronal nets in a tauopathy mouse model

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Kudo, Takehiro, Takuwa, Hiroyuki, Takahashi, Manami, Urushihata, Takuya, Shimojo, Masafumi, Sampei, Kazuaki, Yamanaka, Mitsugu, Tomita, Yutaka +3 more·2023·iScience

Abstract

In Alzheimer's disease (AD), network hyperexcitability is frequently observed and associated with subsequent cognitive impairment. Dysfunction of inhibitory interneurons (INs) is thought to be one of the key biological mechanisms of hyperexcitability. However, it is still unknown how INs are functionally affected in tau pathology, which is a major pathology in AD. To clarify this, we evaluated the neuronal activity of cortical INs in 6-month-old rTg4510 mice, a model of tauopathy. Calcium imaging with mDlx enhancer-driven labeling revealed that neuronal activity in INs was decreased in rTg4510 mice. In the patch clamp recording, the firing properties of fast-spiking INs were altered so as to reduce their activity in rTg4510 mice. In parallel with microglial activation, perineuronal nets around parvalbumin-positive INs were partially disrupted in rTg4510 mice. Taken together, our data indicate that the excitability of cortical fast-spiking INs is decreased, possibly because of the disruption of perineuronal nets.

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  • A recent study performed in 3-month-old and 6-month-old rTg4510 (P301L) mice showed an age-associated decrease in cortical WFA+ PNNs only after the accumulation of pTau and gliosis.

    “A recent study performed in 3-month-old and 6-month-old rTg4510 (P301L) mice, a mouse model of tauopathy associated with familial frontotemporal dementia, showed an age-associated decrease in cortical WFA+ PNNs only after the accumulation of pTau and gliosis (Kudo et al. 2023).”

    From Perineuronal net deglycosylation associates with tauopathy‐induced gliosis and neurodegeneration (2024) · cites this paper as Kudo et al. 2023

    The Results section on perineuronal nets (page unavailable) reports significantly reduced WFA-labeling intensity in the somatosensory cortex of 6-month-old rTg4510 mice, but only a slight reduction at 3 months. The Results also report increased microglia and accumulated hyperphosphorylated tau at 6 months. They do not establish that the PNN change occurred only *after* those changes; the paper describes it as occurring in parallel with microglial activation. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • The rTg4510 study implicates pTau and/or gliosis as a driver for PNN CS-GAG loss.

    “Although this study implicates pTau and/or gliosis as a driver for PNN CS-GAG loss, core protein abundance was not examined.”

    From Perineuronal net deglycosylation associates with tauopathy‐induced gliosis and neurodegeneration (2024) · cites this paper as Kudo et al. 2023

    The Results section reports reduced WFA labeling of PNNs in six-month-old rTg4510 mice, alongside microglial activation. The Discussion suggests that glial proteases might mediate PNN degradation as tau pathology progresses, but it does not establish pTau or gliosis as a causal driver or specifically measure CS-GAG loss. No page numbers are available in our copy. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • In the rTg4510 study, core protein abundance was not examined.

    “core protein abundance was not examined.”

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  1. [1]Jack C.R. Knopman D.S. Jagust W.J. Shaw L.M. Aisen P.S. Weiner M.W. Petersen R.C. Trojanowski J.Q. Hypothetical model of dynamic biomarkers of the Alzheimer’s pathological cascade Lancet Neurol. 9 2010 119 128 10.1016/S1474-4422(09)70299-6 20083042 PMC2819840 · DOI · Paper page
  2. [2]Wu J.W. Hussaini S.A. Bastille I.M. Rodriguez G.A. Mrejeru A. Rilett K. Sanders D.W. Cook C. Fu H. Boonen R.A.C.M. Neuronal activity enhances tau propagation and tau pathology in vivo Nat. Neurosci. 19 2016 1085 1092 10.1038/nn.4328 27322420 PMC4961585 · DOI · Paper page
  3. [3]Vossel K.A. Tartaglia M.C. Nygaard H.B. Zeman A.Z. Miller B.L. Epileptic activity in Alzheimer’s disease: causes and clinical relevance Lancet Neurol. 16 2017 311 322 10.1016/S1474-4422(17)30044-3 28327340 PMC5973551 · DOI · Paper page
  4. [4]Sanchez P.E. Zhu L. Verret L. Vossel K.A. Orr A.G. Cirrito J.R. Devidze N. Ho K. Yu G.Q. Palop J.J. Mucke L. Levetiracetam suppresses neuronal network dysfunction and reverses synaptic and cognitive deficits in an Alzheimer’s disease model Proc. Natl. Acad. Sci. USA 109 2012 E2895 E2903 10.1073/pnas.1121081109 22869752 PMC3479491 · DOI · Paper page
  5. [5]Palop J.J. Mucke L. Network abnormalities and interneuron dysfunction in Alzheimer disease Nat. Rev. Neurosci. 17 2016 777 792 10.1038/nrn.2016.141 27829687 PMC8162106 · DOI · Paper page
  6. [7]Ogiwara I. Miyamoto H. Morita N. Atapour N. Mazaki E. Inoue I. Takeuchi T. Itohara S. Yanagawa Y. Obata K. Nav1.1 localizes to axons of parvalbumin-positive inhibitory interneurons: a circuit basis for epileptic seizures in mice carrying an Scn1a gene mutation J. Neurosci. 27 2007 5903 5914 10.1523/JNEUROSCI.5270-06.2007 17537961 PMC6672241 · DOI · Paper page
  7. [8]Martinez-Losa M. Tracy T.E. Ma K. Verret L. Clemente-Perez A. Khan A.S. Cobos I. Ho K. Gan L. Mucke L. Nav1.1-Overexpressing interneuron transplants restore brain rhythms and cognition in a mouse model of alzheimer’s disease Neuron 98 2018 75 89.e5 10.1016/j.neuron.2018.02.029 29551491 PMC5886814 · DOI
  8. [9]Verret L. Mann E.O. Hang G.B. Barth A.M.I. Cobos I. Ho K. Devidze N. Masliah E. Kreitzer A.C. Mody I. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model Cell 149 2012 708 721 10.1016/j.cell.2012.02.046 22541439 PMC3375906 · DOI · Paper page
  9. [10]Hou X. Yoshioka N. Tsukano H. Sakai A. Miyata S. Watanabe Y. Yanagawa Y. Sakimura K. Takeuchi K. Kitagawa H. Chondroitin sulfate is required for onset and offset of critical period plasticity in visual cortex Sci. Rep. 7 2017 12646 10.1038/s41598-017-04007-x 28974755 PMC5626782 · DOI
  10. [11]Wingert J.C. Sorg B.A. Impact of perineuronal nets on electrophysiology of parvalbumin interneurons, principal neurons, and brain oscillations: a Review Front. Synaptic Neurosci. 13 2021 673210 10.3389/fnsyn.2021.673210 34040511 PMC8141737 · DOI · Paper page
  11. [14]Favuzzi E. Marques-Smith A. Deogracias R. Winterflood C.M. Sánchez-Aguilera A. Mantoan L. Maeso P. Fernandes C. Ewers H. Rico B. Activity-dependent gating of parvalbumin interneuron function by the perineuronal net protein brevican Neuron 95 2017 639 655.e10 10.1016/j.neuron.2017.06.028 28712654 · DOI · Paper page
  12. [15]Xiao Z.C. Ragsdale D.S. Malhotra J.D. Mattei L.N. Braun P.E. Schachner M. Isom L.L. Tenascin-R is a functional modulator of sodium channel β subunits J. Biol. Chem. 274 1999 26511 26517 10.1074/jbc.274.37.26511 10473612 · DOI
  13. [16]Crapser J.D. Arreola M.A. Tsourmas K.I. Green K.N. Microglia as hackers of the matrix: sculpting synapses and the extracellular space Cell. Mol. Immunol. 18 2021 2472 2488 10.1038/s41423-021-00751-3 34413489 PMC8546068 · DOI · Paper page
  14. [17]Crapser J.D. Spangenberg E.E. Barahona R.A. Arreola M.A. Hohsfield L.A. Green K.N. Microglia facilitate loss of perineuronal nets in the Alzheimer’s disease brain EBioMedicine 58 2020 102919 10.1016/j.ebiom.2020.102919 32745992 PMC7399129 · DOI · Paper page
  15. [18]Crapser J.D. Ochaba J. Soni N. Reidling J.C. Thompson L.M. Green K.N. Microglial depletion prevents extracellular matrix changes and striatal volume reduction in a model of Huntington’s disease Brain 143 2020 266 288 10.1093/brain/awz363 31848580 PMC6935750 · DOI · Paper page
  16. [19]Maeda J. Minamihisamatsu T. Shimojo M. Zhou X. Ono M. Matsuba Y. Ji B. Ishii H. Ogawa M. Akatsu H. Distinct microglial response against Alzheimer’s amyloid and tau pathologies characterized by P2Y12 receptor Brain Commun. 3 2021 fcab011 10.1093/braincomms/fcab011 33644757 PMC7901060 · DOI
  17. [20]Takado Y. Takuwa H. Sampei K. Urushihata T. Takahashi M. Shimojo M. Uchida S. Nitta N. Shibata S. Nagashima K. MRS-measured glutamate versus GABA reflects excitatory versus inhibitory neural activities in awake mice J. Cereb. Blood Flow Metab. 42 2022 197 212 10.1177/0271678X211045449 34515548 PMC8721779 · DOI
  18. [21]Dimidschstein J. Chen Q. Tremblay R. Rogers S.L. Saldi G.A. Guo L. Xu Q. Liu R. Lu C. Chu J. A viral strategy for targeting and manipulating interneurons across vertebrate species Nat. Neurosci. 19 2016 1743 1749 10.1038/nn.4430 27798629 PMC5348112 · DOI · Paper page
  19. [22]Adibi M. Whisker-mediated Touch system in rodents: from neuron to behavior Front. Syst. Neurosci. 13 2019 40 10.3389/fnsys.2019.00040 31496942 PMC6712080 · DOI
  20. [23]Yu J. Hu H. Agmon A. Svoboda K. Recruitment of GABAergic interneurons in the barrel cortex during active tactile behavior Neuron 104 2019 412 427.e4 10.1016/j.neuron.2019.07.027 31466734 PMC6813892 · DOI
  21. [24]Avermann M. Tomm C. Mateo C. Gerstner W. Petersen C.C.H. Microcircuits of excitatory and inhibitory neurons in layer 2/3 of mouse barrel cortex J. Neurophysiol. 107 2012 3116 3134 10.1152/jn.00917.2011 22402650 · DOI
  22. [25]Rudy B. Chow A. Lau D. Amarillo Y. Ozaita A. Saganich M. Moreno H. Nadal M.S. Hernandez-Pineda R. Hernandez-Cruz A. Contributions of Kv3 channels to neuronal excitability Ann.N. Y. Acad. Sci. 868 1999 304 343 10.1111/j.1749-6632.1999.tb11295.x 10414303 · DOI · Paper page
  23. [26]Crimins J.L. Rocher A.B. Luebke J.I. Electrophysiological changes precede morphological changes to frontal cortical pyramidal neurons in the rTg4510 mouse model of progressive tauopathy Acta Neuropathol. 124 2012 777 795 10.1007/s00401-012-1038-9 22976049 PMC3509230 · DOI
  24. [27]Dalby N.O. Volbracht C. Helboe L. Larsen P.H. Jensen H.S. Egebjerg J. Elvang A.B. Altered function of hippocampal CA1 pyramidal neurons in the rTg4510 mouse model of tauopathy J. Alzheimers Dis. 40 2014 429 442 10.3233/JAD-131358 24448785 · DOI
  25. [28]Hatch R.J. Wei Y. Xia D. Götz J. Hyperphosphorylated tau causes reduced hippocampal CA1 excitability by relocating the axon initial segment Acta Neuropathol. 133 2017 717 730 10.1007/s00401-017-1674-1 28091722 PMC5389999 · DOI
  26. [29]Santacruz K. Lewis J. Spires T. Paulson J. Kotilinek L. Ingelsson M. Guimaraes A. DeTure M. Ramsden M. McGowan E. Medicine: tau suppression in a neurodegenerative mouse model improves memory function Science 309 2005 476 481 10.1126/science.1113694 16020737 PMC1574647 · DOI · Paper page
  27. [30]Ramsden M. Kotilinek L. Forster C. Paulson J. McGowan E. SantaCruz K. Guimaraes A. Yue M. Lewis J. Carlson G. Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L) J. Neurosci. 25 2005 10637 10647 10.1523/JNEUROSCI.3279-05.2005 16291936 PMC6725849 · DOI · Paper page
  28. [31]Holmes H.E. Powell N.M. Ma D. Ismail O. Harrison I.F. Wells J.A. Colgan N. O’Callaghan J.M. Johnson R.A. Murray T.K. Comparison of in vivo and Ex vivo MRI for the detection of structural abnormalities in a mouse model of tauopathy Front. Neuroinform. 11 2017 20 10.3389/fninf.2017.00020 28408879 PMC5374887 · DOI · Paper page
  29. [32]Gu Y. Servello D. Han Z. Lalchandani R.R. Ding J.B. Huang K. Gu C. Balanced activity between Kv3 and Nav channels determines fast-spiking in mammalian central neurons iScience 9 2018 120 137 10.1016/j.isci.2018.10.014 30390433 PMC6218699 · DOI
  30. [33]Weiser M. Bueno E. Sekirnjak C. Martone M.E. Baker H. Hillman D. Chen S. Thornhill W. Ellisman M. Rudy B. The potassium channel subunit KV3.1b is localized to somatic and axonal membranes of specific populations of CNS neurons J. Neurosci. 15 1995 4298 4314 10.1523/jneurosci.15-06-04298.1995 7790912 PMC6577740 · DOI
  31. [34]Lensjø K.K. Christensen A.C. Tennøe S. Fyhn M. Hafting T. Differential expression and cell-type specificity of perineuronal nets in hippocampus, medial entorhinal cortex, and visual cortex examined in the rat and mouse eNeuro 4 2017 10.1523/ENEURO.0379-16.2017 ENEURO.0379-16.2017 PMC5461557 28593193 · DOI · Paper page
  32. [35]Sobue A. Komine O. Hara Y. Endo F. Mizoguchi H. Watanabe S. Murayama S. Saito T. Saido T.C. Sahara N. Microglial gene signature reveals loss of homeostatic microglia associated with neurodegeneration of Alzheimer’s disease Acta Neuropathol. Commun. 9 2021 1 10.1186/s40478-020-01099-x 33402227 PMC7786928 · DOI · Paper page
  33. [36]Nguyen P.T. Dorman L.C. Pan S. Vainchtein I.D. Han R.T. Nakao-Inoue H. Taloma S.E. Barron J.J. Molofsky A.B. Kheirbek M.A. Microglial remodeling of the extracellular matrix promotes synapse plasticity Cell 182 2020 388 403.e15 10.1016/j.cell.2020.05.050 32615087 PMC7497728 · DOI · Paper page
  34. [38]Pirbhoy P.S. Rais M. Lovelace J.W. Woodard W. Razak K.A. Binder D.K. Ethell I.M. Acute pharmacological inhibition of matrix metalloproteinase-9 activity during development restores perineuronal net formation and normalizes auditory processing in Fmr1 KO mice J. Neurochem. 155 2020 538 558 10.1111/jnc.15037 32374912 PMC7644613 · DOI · Paper page
  35. [39]Hao H.P. Doh-Ura K. Nakanishi H. Impairment of microglial responses to facial nerve axotomy in cathepsin S-deficient mice J. Neurosci. Res. 85 2007 2196 2206 10.1002/jnr.21357 17539023 · DOI
  36. [40]Petanceska S. Canoll P. Devi L.A. Expression of rat cathepsin S in phagocytic cells J. Biol. Chem. 271 1996 4403 4409 10.1074/jbc.271.8.4403 8626791 · DOI
  37. [41]Pantazopoulos H. Gisabella B. Rexrode L. Benefield D. Yildiz E. Seltzer P. Valeri J. Chelini G. Reich A. Ardelt M. Circadian rhythms of perineuronal net composition eNeuro 7 2020 10.1523/ENEURO.0034-19.2020 ENEURO.0034-19.2020 PMC7405073 32719104 · DOI
  38. [42]Wen T.H. Binder D.K. Ethell I.M. Razak K.A. The perineuronal ‘safety’ net? Perineuronal net abnormalities in neurological disorders Front. Mol. Neurosci. 11 2018 270 10.3389/fnmol.2018.00270 30123106 PMC6085424 · DOI · Paper page
  39. [43]Lemarchant S. Pomeshchik Y. Kidin I. Kärkkäinen V. Valonen P. Lehtonen S. Goldsteins G. Malm T. Kanninen K. Koistinaho J. ADAMTS-4 promotes neurodegeneration in a mouse model of amyotrophic lateral sclerosis Mol. Neurodegener. 11 2016 10 10.1186/s13024-016-0078-3 26809777 PMC4727317 · DOI
  40. [45]Vossel K.A. Ranasinghe K.G. Beagle A.J. Mizuiri D. Honma S.M. Dowling A.F. Darwish S.M. van Berlo V. Barnes D.E. Mantle M. Incidence and impact of subclinical epileptiform activity in Alzheimer’s disease Ann. Neurol. 80 2016 858 870 10.1002/ana.24794 27696483 PMC5177487 · DOI · Paper page
  41. [46]Palop J.J. Chin J. Roberson E.D. Wang J. Thwin M.T. Bien-Ly N. Yoo J. Ho K.O. Yu G.Q. Kreitzer A. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer’s disease Neuron 55 2007 697 711 10.1016/j.neuron.2007.07.025 17785178 PMC8055171 · DOI · Paper page
  42. [47]Xu Y. Zhao M. Han Y. Zhang H. GABAergic inhibitory interneuron deficits in alzheimer’s disease: implications for treatment Front. Neurosci. 14 2020 660 10.3389/fnins.2020.00660 32714136 PMC7344222 · DOI · Paper page
  43. [48]Jackson J.S. Witton J. Johnson J.D. Ahmed Z. Ward M. Randall A.D. Hutton M.L. Isaac J.T. O’Neill M.J. Ashby M.C. Altered synapse stability in the early stages of tauopathy Cell Rep. 18 2017 3063 3068 10.1016/j.celrep.2017.03.013 28355559 PMC5382238 · DOI
  44. [49]Hu T. Xiao Z. Mao R. Chen B. Lu M.N. Tong J. Mei R. Li S.S. Xiao Z.C. Zhang L.F. Xiyang Y.B. Navβ2 knockdown improves cognition in APP/PS1 mice by partially inhibiting seizures and APP amyloid processing Oncotarget 8 2017 99284 99295 10.18632/oncotarget.21849 29245901 PMC5725092 · DOI
  45. [50]Hamm V. Héraud C. Bott J.B. Herbeaux K. Strittmatter C. Mathis C. Goutagny R. Differential contribution of APP metabolites to early cognitive deficits in a TgCRND8 mouse model of Alzheimer’s disease Sci. Adv. 3 2017 e1601068 10.1126/sciadv.1601068 28275722 PMC5325539 · DOI
  46. [51]Fukumoto H. Cheung B.S. Hyman B.T. Irizarry M.C. β-secretase protein and activity are increased in the neocortex in Alzheimer disease Arch. Neurol. 59 2002 1381 1389 10.1001/archneur.59.9.1381 12223024 · DOI
  47. [52]Tyler S.J. Dawbarn D. Wilcock G.K. Allen S.J. α- and β-secretase: profound changes in Alzheimer’s disease Biochem. Biophys. Res. Commun. 299 2002 373 376 10.1016/S0006-291X(02)02635-9 12445809 · DOI
  48. [53]Yang L.B. Lindholm K. Yan R. Citron M. Xia W. Yang X.L. Beach T. Sue L. Wong P. Price D. Elevated β-secretase expression and enzymatic activity detected in sporadic Alzheimer disease [1] Nat. Med. 9 2003 3 4 10.1038/nm0103-3 12514700 · DOI · Paper page
  49. [54]Holsinger R.M.D. McLean C.A. Beyreuther K. Masters C.L. Evin G. Increased expression of the amyloid precursor β-secretase in Alzheimer’s disease Ann. Neurol. 51 2002 783 786 10.1002/ana.10208 12112088 · DOI · Paper page
  50. [55]Li R. Lindholm K. Yang L.B. Yue X. Citron M. Yan R. Beach T. Sue L. Sabbagh M. Cai H. Amyloid β peptide load is correlated with increased β-secretase activity in sporadic Alzheimer’s disease patients Proc. Natl. Acad. Sci. USA 101 2004 3632 3637 10.1073/pnas.0205689101 14978286 PMC373514 · DOI
  51. [56]Corbett B.F. Leiser S.C. Ling H.P. Nagy R. Breysse N. Zhang X. Hazra A. Brown J.T. Randall A.D. Wood A. Sodium channel cleavage is associated with aberrant neuronal activity and cognitive deficits in a mouse model of alzheimer’s disease J. Neurosci. 33 2013 7020 7026 10.1523/JNEUROSCI.2325-12.2013 23595759 PMC6618875 · DOI
  52. [57]Zhao J. Fu Y. Yasvoina M. Shao P. Hitt B. O’Connor T. Logan S. Maus E. Citron M. Berry R. β-site amyloid precursor protein cleaving enzyme 1 levels become elevated in neurons around amyloid plaques: implications for Alzheimer’s disease pathogenesis J. Neurosci. 27 2007 3639 3649 10.1523/JNEUROSCI.4396-06.2007 17409228 PMC6672403 · DOI · Paper page
  53. [58]Kim D.Y. Carey B.W. Wang H. Ingano L.A.M. Binshtok A.M. Wertz M.H. Pettingell W.H. He P. Lee V.M.Y. Woolf C.J. Kovacs D.M. BACE1 regulates voltage-gated sodium channels and neuronal activity Nat. Cell Biol. 9 2007 755 764 10.1038/ncb1602 17576410 PMC2747787 · DOI
  54. [60]Saito T. Matsuba Y. Yamazaki N. Hashimoto S. Saido T.C. Calpain activation in Alzheimer’s model mice is an artifact of APP and presenilin overexpression J. Neurosci. 36 2016 9933 9936 10.1523/JNEUROSCI.1907-16.2016 27656030 PMC5030353 · DOI · Paper page
  55. [61]Stevens S.R. Longley C.M. Ogawa Y. Teliska L.H. Arumanayagam A.S. Nair S. Oses-Prieto J.A. Burlingame A.L. Cykowski M.D. Xue M. Rasband M.N. Ankyrin-r regulates fast-spiking interneuron excitability through perineuronal nets and Kv3.1b K+ channels Elife 10 2021 e66491 10.7554/eLife.66491 34180393 PMC8257253 · DOI · Paper page
  56. [62]Suttkus A. Rohn S. Weigel S. Glöckner P. Arendt T. Morawski M. Aggrecan, link protein and tenascin-R are essential components of the perineuronal net to protect neurons against iron-induced oxidative stress Cell Death Dis. 5 2014 e1119 10.1038/cddis.2014.25 24625978 PMC3973247 · DOI · Paper page
  57. [63]Srinivasan J. Schachner M. Catterall W.A. Interaction of voltage-gated sodium channels with the extracellular matrix molecules tenascin-C and tenascin-R Proc. Natl. Acad. Sci. USA 95 1998 15753 15757 10.1073/pnas.95.26.15753 9861042 PMC28116 · DOI
  58. [64]Liu Y.J. Spangenberg E.E. Tang B. Holmes T.C. Green K.N. Xu X. Microglia elimination increases neural circuit connectivity and activity in adult mouse cortex J. Neurosci. 41 2021 1274 1287 10.1523/JNEUROSCI.2140-20.2020 33380470 PMC7888230 · DOI
  59. [65]Venturino A. Schulz R. De Jesús-Cortés H. Maes M.E. Nagy B. Reilly-Andújar F. Colombo G. Cubero R.J.A. Schoot Uiterkamp F.E. Bear M.F. Siegert S. Microglia enable mature perineuronal nets disassembly upon anesthetic ketamine exposure or 60-Hz light entrainment in the healthy brain Cell Rep. 36 2021 109313 10.1016/j.celrep.2021.109313 34233180 PMC8284881 · DOI · Paper page
  60. [66]Baig S. Wilcock G.K. Love S. Loss of perineuronal net N-acetylgalactosamine in Alzheimer’s disease Acta Neuropathol. 110 2005 393 401 10.1007/s00401-005-1060-2 16133543 · DOI · Paper page
  61. [67]Lemere C.A. Munger J.S. Shi G.P. Natkin L. Haass C. Chapman H.A. Selkoe D.J. The lysosomal cysteine protease, cathepsin S, is increased in Alzheimer’s disease and Down syndrome brain: an immunocytochemical study Am. J. Pathol. 146 1995 848 860 7717452 PMC1869262
  62. [68]Hernandes-Alejandro M. Montaño S. Harrington C.R. Wischik C.M. Salas-Casas A. Cortes-Reynosa P. Pérez Salazar E. Cazares-Apatiga J. Apatiga-Perez R. Ontiveros Torres M.Á. Analysis of the relationship between metalloprotease-9 and tau protein in alzheimer’s disease J. Alzheimers Dis. 76 2020 553 569 10.3233/JAD-200146 32538846 · DOI
  63. [69]Langenfurth A. Rinnenthal J.L. Vinnakota K. Prinz V. Carlo A.S. Stadelmann C. Siffrin V. Peaschke S. Endres M. Heppner F. Membrane-type 1 metalloproteinase is upregulated in microglia/brain macrophages in neurodegenerative and neuroinflammatory diseases J. Neurosci. Res. 92 2014 275 286 10.1002/jnr.23288 24323769 · DOI
  64. [70]Py N.A. Bonnet A.E. Bernard A. Marchalant Y. Charrat E. Checler F. Khrestchatisky M. Baranger K. Rivera S. Differential spatio-temporal regulation of MMPs in the 5xFAD mouse model of Alzheimer’s disease: evidence for a pro-amyloidogenic role of MT1-MMP Front. Aging Neurosci. 6 2014 247 10.3389/fnagi.2014.00247 25278878 PMC4166961 · DOI
  65. [71]Nagy V. Bozdagi O. Matynia A. Balcerzyk M. Okulski P. Dzwonek J. Costa R.M. Silva A.J. Kaczmarek L. Huntley G.W. Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory J. Neurosci. 26 2006 1923 1934 10.1523/JNEUROSCI.4359-05.2006 16481424 PMC4428329 · DOI · Paper page
  66. [72]Wes P.D. Easton A. Corradi J. Barten D.M. Devidze N. DeCarr L.B. Truong A. He A. Barrezueta N.X. Polson C. Tau overexpression impacts a neuroinflammation gene expression network perturbed in Alzheimer’s disease PLoS One 9 2014 e106050 10.1371/journal.pone.0106050 25153994 PMC4143352 · DOI
  67. [73]Ribot J. Breton R. Calvo C.F. Moulard J. Ezan P. Zapata J. Samama K. Moreau M. Bemelmans A.P. Sabatet V. Astrocytes close the mouse critical period for visual plasticity Science 373 2021 77 81 10.1126/science.abf5273 34210880 · DOI
  68. [74]Foster J.B. Lashley R. Zhao F. Wang X. Kung N. Askwith C.C. Lin L. Shultis M.W. Hodgetts K.J. Lin C.L.G. Enhancement of tripartite synapses as a potential therapeutic strategy for Alzheimer’s disease: a preclinical study in rTg4510 mice Alzheimer's Res. Ther. 11 2019 75 10.1186/s13195-019-0530-z 31439023 PMC6706914 · DOI
  69. [75]Zhou L. McInnes J. Wierda K. Holt M. Herrmann A.G. Jackson R.J. Wang Y.C. Swerts J. Beyens J. Miskiewicz K. Tau association with synaptic vesicles causes presynaptic dysfunction Nat. Commun. 8 2017 15295 10.1038/ncomms15295 28492240 PMC5437271 · DOI · Paper page
  70. [76]Gelman S. Palma J. Tombaugh G. Ghavami A. Differences in synaptic dysfunction between rTg4510 and APP/PS1 mouse models of alzheimer’s disease J. Alzheimers Dis. 61 2018 195 208 10.3233/JAD-170457 29154272 PMC5836403 · DOI
  71. [77]Putra M. Puttachary S. Liu G. Lee G. Thippeswamy T. Fyn-tau ablation modifies PTZ-induced seizures and post-seizure hallmarks of early epileptogenesis Front. Cell. Neurosci. 14 2020 592374 10.3389/fncel.2020.592374 33363455 PMC7752812 · DOI
  72. [78]Sampei K. Seki C. Takuwa H. Maeda J. Ono M. Tokunaga M. Shimojo M. Honda S. Kimura T. Ishikawa T. Activation of Nav1.1 ameliorates tau pathology and brain atrophy in a mouse model of tauopathy Alzheimer’s Dement 16 2020 e038201 10.1002/alz.038201 · DOI
  73. [79]Gamache J. Benzow K. Forster C. Kemper L. Hlynialuk C. Furrow E. Ashe K.H. Koob M.D. Factors other than hTau overexpression that contribute to tauopathy-like phenotype in rTg4510 mice Nat. Commun. 10 2019 2479 10.1038/s41467-019-10428-1 31171783 PMC6554306 · DOI
  74. [80]Ishikawa A. Tokunaga M. Maeda J. Minamihisamatsu T. Shimojo M. Takuwa H. Ono M. Ni R. Hirano S. Kuwabara S. In vivo visualization of tau accumulation, microglial activation, and brain atrophy in a mouse model of tauopathy rTg4510 J. Alzheimers Dis. 61 2018 1037 1052 10.3233/JAD-170509 29332041 · DOI
  75. [81]Schindelin J. Arganda-Carreras I. Frise E. Kaynig V. Longair M. Pietzsch T. Preibisch S. Rueden C. Saalfeld S. Schmid B. Fiji: an open-source platform for biological-image analysis Nat. Methods 9 2012 676 682 10.1038/nmeth.2019 22743772 PMC3855844 · DOI · Paper page
  76. [82]McClure C. Cole K.L.H. Wulff P. Klugmann M. Murray A.J. Production and titering of recombinant adeno-associated viral vectors J. Vis. Exp. 57 2011 e3348 10.3791/3348 PMC3308604 22143312 · DOI
  77. [83]Tomita Y. Kubis N. Calando Y. Tran Dinh A. Méric P. Seylaz J. Pinard E. Long-term in vivo investigation of mouse cerebral microcirculation by fluorescence confocal microscopy in the area of focal ischemia J. Cereb. Blood Flow Metab. 25 2005 858 867 10.1038/sj.jcbfm.9600077 15758950 · DOI
  78. [84]Pnevmatikakis E.A. Giovannucci A. NoRMCorre: an online algorithm for piecewise rigid motion correction of calcium imaging data J. Neurosci. Methods 291 2017 83 94 10.1016/j.jneumeth.2017.07.031 28782629 · DOI
  79. [85]Jia H. Rochefort N.L. Chen X. Konnerth A. In vivo two-photon imaging of sensory-evoked dendritic calcium signals in cortical neurons Nat. Protoc. 6 2011 28 35 10.1038/nprot.2010.169 21212780 · DOI
  80. [86]Sahara N. Murayama M. Higuchi M. Suhara T. Takashima A. Biochemical distribution of tau protein in synaptosomal fraction of transgenic mice expressing human p301l tau Front. Neurol. 5 2014 26 10.3389/fneur.2014.00026 24653715 PMC3949102 · DOI
  81. [87]Pfaffl M.W. A new mathematical model for relative quantification in real-time RT–PCR Nucleic Acids Res. 29 2001 e45 10.1093/nar/29.9.e45 11328886 PMC55695 · DOI · Paper page

Cited by

Sorted by citations

Authors
Kudo, T., Takuwa, H., Takahashi, M., Urushihata, T., Shimojo, M., Sampei, K., Yamanaka, M., Tomita, Y., Sahara, N., Suhara, T., & Higuchi, M.
Affiliations
  • Tohoku University (JP)
  • National Institutes for Quantum Science and Technology (JP)
  • Sumitomo Dainippon Pharma (Japan) (JP)
Corresponding author
  • Takuwa, Hiroyuki
  • Higuchi, Makoto
Venue
iScience
Publisher
Elsevier BV
Published
2023-04
Volume
26
Issue
4
Pages
106342
ISSN
2589-0042 (ISSN-L)
OpenAlex
W4323257053
Cited by
16
References
6
Citations by year
2026: 2 · 2025: 5 · 2024: 7 · 2023: 2
FWCI
2.84
Type
journal article
Language
en
Open access
Locations
  • iScience (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Institutional Repositories DataBase (IRDB) (submittedVersion)
  • QST-Repository (National Institutes for Quantum and Radiological Science and Technology) (submittedVersion, cc-by-nc-nd)
  • QST-Repository (National Institutes for Quantum and Radiological Science and Technology) (submittedVersion)
Funders
  • Japan Agency for Medical Research and Development (19dk0207049)
  • JSPS
  • Japan Society for the Promotion of Science (21H05705)
Topics
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
perineuronal nets, tauopathy, Alzheimer's disease, rTg4510 mice, network hyperexcitability, parvalbumin interneurons, microglial activation, neuronal excitability, calcium imaging

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