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Tau depletion prevents progressive blood-brain barrier damage in a mouse model of tauopathy

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Blair, Laura J, Frauen, Haley D, Zhang, Bo, Nordhues, Bryce A, Bijan, Sara, Lin, Yen-Chi, Zamudio, Frank, Hernandez, Lidice D +3 more·2015·Acta Neuropathologica Communications
DOI 10.1186/s40478-015-0186-2PMC PMC4353464
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Abstract

INTRODUCTION: The blood-brain barrier (BBB) is damaged in tauopathies, including progressive supranuclear palsy (PSP) and Alzheimer's disease (AD), which is thought to contribute to pathogenesis later in the disease course. In AD, BBB dysfunction has been associated with amyloid beta (Aß) pathology, but the role of tau in this process is not well characterized. Since increased BBB permeability is found in tauopathies without Aß pathology, like PSP, we suspected that tau accumulation alone could not only be sufficient, but even more important than Aß for BBB damage. RESULTS: Longitudinal evaluation of brain tissue from the tetracycline-regulatable rTg4510 tau transgenic mouse model showed progressive IgG, T cell and red blood cell infiltration. The Evans blue (EB) dye that is excluded from the brain when the BBB is intact also permeated the brains of rTg4510 mice following peripheral administration, indicative of a bonafide BBB defect, but this was only evident later in life. Thus, despite the marked brain atrophy and inflammation that occurs earlier in this model, BBB integrity is maintained. Interestingly, BBB dysfunction emerged at the same time that perivascular tau emerged around major hippocampal blood vessels. However, when tau expression was suppressed using doxycycline, BBB integrity was preserved, suggesting that the BBB can be stabilized in a tauopathic brain by reducing tau levels. CONCLUSIONS: For the first time, these data demonstrate that tau alone can initiate breakdown of the BBB, but the BBB is remarkably resilient, maintaining its integrity in the face of marked brain atrophy, neuroinflammation and toxic tau accumulation. Moreover, the BBB can recover integrity when tau levels are reduced. Thus, late stage interventions targeting tau may slow the vascular contributions to cognitive impairment and dementia that occur in tauopathies.

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  • Tau transgenic models (TetO-Tau P301L) also exhibit BBB leakage, microbleeds, IgG deposits, and leukocyte infiltration detected before tau pathology and with no evidence of Aβ pathology.

    “Additionally, tau transgenic models ( TetO-Tau P301L ) also exhibit BBB leakage, microbleeds, IgG deposits, and leukocyte infiltration detected before tau pathology and with no evidence of A 𝛃 pathology (66), supporting that cerebrovascular dysfunction contributes to AD progression.”

    From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [66]

    The Abstract (Results) and Results sections report BBB leakage, IgG deposits, and red blood cell and T-cell infiltration in aged rTg4510 mice. But the Discussion says BBB dysfunction appeared after tau accumulation and alongside perivascular tau—not before tau pathology. The Introduction discusses tauopathies without Aβ overproduction, but the cited passages do not establish an absence of Aβ pathology in these mice. (LLM, conf=0.90)

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  1. [1]Broadwell RD Salcman M Expanding the definition of the blood-brain barrier to protein Proc Natl Acad Sci U S A 1981 78 12 7820 7824 10.1073/pnas.78.12.7820 6950422 PMC349363 · DOI
  2. [2]Wenkel H Streilein JW Young MJ Systemic immune deviation in the brain that does not depend on the integrity of the blood-brain barrier J Immunol 2000 164 10 5125 5131 10.4049/jimmunol.164.10.5125 10799870 · DOI
  3. [3]Mooradian AD Effect of aging on the blood-brain barrier Neurobiol Aging 1988 9 1 31 39 10.1016/S0197-4580(88)80013-7 3288893 · DOI
  4. [4]Marques F Sousa JC Sousa N Palha JA Blood-brain-barriers in aging and in Alzheimer's disease Mol Neurodegener 2013 8 38 10.1186/1750-1326-8-38 24148264 PMC4015275 · DOI
  5. [5]Sengillo JD Winkler EA Walker CT Sullivan JS Johnson M Zlokovic BV Deficiency in mural vascular cells coincides with blood-brain barrier disruption in Alzheimer's disease Brain Pathol 2013 23 3 303 310 10.1111/bpa.12004 23126372 PMC3628957 · DOI · Paper page
  6. [6]Viggars AP Wharton SB Simpson JE Matthews FE Brayne C Savva GM Garwood C Drew D Shaw PJ Ince PG Alterations in the blood brain barrier in ageing cerebral cortex in relationship to Alzheimer-type pathology: a study in the MRC-CFAS population neuropathology cohort Neurosci Lett 2011 505 1 25 30 10.1016/j.neulet.2011.09.049 21970975 · DOI
  7. [7]Bowman GL Kaye JA Moore M Waichunas D Carlson NE Quinn JF Blood-brain barrier impairment in Alzheimer disease: stability and functional significance Neurology 2007 68 21 1809 1814 10.1212/01.wnl.0000262031.18018.1a 17515542 PMC2668699 · DOI
  8. [9]Sharma HS Castellani RJ Smith MA Sharma A The blood-brain barrier in Alzheimer's disease: novel therapeutic targets and nanodrug delivery Int Rev Neurobiol 2012 102 47 90 10.1016/B978-0-12-386986-9.00003-X 22748826 · DOI
  9. [12]Oshima K Uchikado H Dickson DW Perivascular neuritic dystrophy associated with cerebral amyloid angiopathy in Alzheimer's disease Int J Clin Exp Pathol 2008 1 5 403 408 18787622 PMC2480573
  10. [13]Wilcock DM Lewis MR Van Nostrand WE Davis J Previti ML Gharkholonarehe N Vitek MP Colton CA Progression of amyloid pathology to Alzheimer's disease pathology in an amyloid precursor protein transgenic mouse model by removal of nitric oxide synthase 2 J Neurosci 2008 28 7 1537 1545 10.1523/JNEUROSCI.5066-07.2008 18272675 PMC2621082 · DOI
  11. [14]Vidal R Calero M Piccardo P Farlow MR Unverzagt FW Mendez E Jimenez-Huete A Beavis R Gallo G Gomez-Tortosa E Ghiso J Hyman BT Frangione B Ghetti B Senile dementia associated with amyloid beta protein angiopathy and tau perivascular pathology but not neuritic plaques in patients homozygous for the APOE-epsilon4 allele Acta Neuropathol 2000 100 1 1 12 10.1007/s004010051186 10912914 · DOI
  12. [15]Bartels AL Willemsen AT Kortekaas R de Jong BM de Vries R de Klerk O van Oostrom JC Portman A Leenders KL Decreased blood-brain barrier P-glycoprotein function in the progression of Parkinson's disease, PSP and MSA J Neural Transm 2008 115 7 1001 1009 10.1007/s00702-008-0030-y 18265929 PMC2468317 · DOI
  13. [16]de Vries HE Kuiper J de Boer AG Van Berkel TJ Breimer DD The blood-brain barrier in neuroinflammatory diseases Pharmacol Rev 1997 49 2 143 155 9228664
  14. [17]Garbuzova-Davis S Hernandez-Ontiveros DG Rodrigues MC Haller E Frisina-Deyo A Mirtyl S Sallot S Saporta S Borlongan CV Sanberg PR Impaired blood-brain/spinal cord barrier in ALS patients Brain Res 2012 1469 114 128 10.1016/j.brainres.2012.05.056 22750125 · DOI
  15. [18]Forman MS Lal D Zhang B Dabir DV Swanson E Lee VM Trojanowski JQ Transgenic mouse model of tau pathology in astrocytes leading to nervous system degeneration J Neurosci 2005 25 14 3539 3550 10.1523/JNEUROSCI.0081-05.2005 15814784 PMC6725385 · DOI · Paper page
  16. [19]Jaworski T Dewachter I Lechat B Croes S Termont A Demedts D Borghgraef P Devijver H Filipkowski RK Kaczmarek L Kugler S Van Leuven F AAV-tau mediates pyramidal neurodegeneration by cell-cycle re-entry without neurofibrillary tangle formation in wild-type mice PLoS ONE 2009 4 10 e7280 10.1371/journal.pone.0007280 19794916 PMC2748684 · DOI
  17. [20]Jaworski T Lechat B Demedts D Gielis L Devijver H Borghgraef P Duimel H Verheyen F Kugler S Van Leuven F Dendritic degeneration, neurovascular defects, and inflammation precede neuronal loss in a mouse model for tau-mediated neurodegeneration Am J Pathol 2011 179 4 2001 2015 10.1016/j.ajpath.2011.06.025 21839061 PMC3181369 · DOI
  18. [21]Kovac A Zilkova M Deli MA Zilka N Novak M Human truncated tau is using a different mechanism from amyloid-beta to damage the blood-brain barrier J Alzheimers Dis 2009 18 4 897 906 19749439
  19. [22]Dickey C Kraft C Jinwal U Koren J Johnson A Anderson L Lebson L Lee D Dickson D de Silva R Binder LI Morgan D Lewis J Aging analysis reveals slowed tau turnover and enhanced stress response in a mouse model of tauopathy Am J Pathol 2009 174 1 228 238 10.2353/ajpath.2009.080764 19074615 PMC2631335 · DOI
  20. [23]Santacruz K Lewis J Spires T Paulson J Kotilinek L Ingelsson M Guimaraes A DeTure M Ramsden M McGowan E Forster C Yue M Orne J Janus C Mariash A Kuskowski M Hyman B Hutton M Ashe KH Tau suppression in a neurodegenerative mouse model improves memory function Science 2005 309 5733 476 481 10.1126/science.1113694 16020737 PMC1574647 · DOI · Paper page
  21. [26]Sahara N DeTure M Ren Y Ebrahim AS Kang D Knight J Volbracht C Pedersen JT Dickson DW Yen SH Lewis J Characteristics of TBS-extractable hyperphosphorylated tau species: aggregation intermediates in rTg4510 mouse brain J Alzheimers Dis 2013 33 1 249 263 22941973 PMC3514650
  22. [27]Sahara N Ren Y Ward S Binder LI Suhara T Higuchi M Tau oligomers as potential targets for early diagnosis of tauopathy J Alzheimers Dis 2014 40 S91 S96 24595194
  23. [28]Rudd PA Bastien-Hamel LE von Messling V Acute canine distemper encephalitis is associated with rapid neuronal loss and local immune activation J Gen Virol 2010 91 Pt 4 980 989 10.1099/vir.0.017780-0 20016033 · DOI
  24. [29]Tetrault S Chever O Sik A Amzica F Opening of the blood-brain barrier during isoflurane anaesthesia Eur J Neurosci 2008 28 7 1330 1341 10.1111/j.1460-9568.2008.06443.x 18973560 · DOI
  25. [30]Gordon MN Schreier WA Ou X Holcomb LA Morgan DG Exaggerated astrocyte reactivity after nigrostriatal deafferentation in the aged rat J Comp Neurol 1997 388 1 106 119 10.1002/(SICI)1096-9861(19971110)388:1<106::AID-CNE7>3.0.CO;2-5 9364241 · DOI
  26. [31]Abisambra JF Blair LJ Hill SE Jones JR Kraft C Rogers J Koren J 3rd Jinwal UK Lawson L Johnson AG Wilcock D O'Leary JC Jansen-West K Muschol M Golde TE Weeber EJ Banko J Dickey CA Phosphorylation dynamics regulate Hsp27-mediated rescue of neuronal plasticity deficits in tau transgenic mice J Neurosci 2010 30 46 15374 15382 10.1523/JNEUROSCI.3155-10.2010 21084594 PMC3073547 · DOI
  27. [32]Fischer AH Jacobson KA Rose J Zeller R Hematoxylin and eosin staining of tissue and cell sections CSH Protocols 2008 2008 pdb prot4986 21356829
  28. [33]Carty N Lee D Dickey C Ceballos-Diaz C Jansen-West K Golde TE Gordon MN Morgan D Nash K Convection-enhanced delivery and systemic mannitol increase gene product distribution of AAV vectors 5, 8, and 9 and increase gene product in the adult mouse brain J Neurosci Methods 2010 194 1 144 153 10.1016/j.jneumeth.2010.10.010 20951738 PMC2995441 · DOI
  29. [35]Pluta R Januszewski S Jablonski M Ulamek M Factors in creepy delayed neuronal death in hippocampus following brain ischemia-reperfusion injury with long-term survival Acta neurochirurgica Suppl 2010 106 37 41 10.1007/978-3-211-98811-4_5 19812917 · DOI
  30. [36]Ueno M Sakamoto H Tomimoto H Akiguchi I Onodera M Huang CL Kanenishi K Blood-brain barrier is impaired in the hippocampus of young adult spontaneously hypertensive rats Acta Neuropathol 2004 107 6 532 538 10.1007/s00401-004-0845-z 15042385 · DOI
  31. [37]Ueno M Akiguchi I Hosokawa M Kotani H Kanenishi K Sakamoto H Blood-brain barrier permeability in the periventricular areas of the normal mouse brain Acta Neuropathol 2000 99 4 385 392 10.1007/s004010051140 10787037 · DOI
  32. [38]Ramsden M Kotilinek L Forster C Paulson J McGowan E SantaCruz K Guimaraes A Yue M Lewis J Carlson G Hutton M Ashe KH Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L) J Neurosci 2005 25 46 10637 10647 10.1523/JNEUROSCI.3279-05.2005 16291936 PMC6725849 · DOI · Paper page
  33. [39]Saria A Lundberg JM Evans blue fluorescence: quantitative and morphological evaluation of vascular permeability in animal tissues J Neurosci Methods 1983 8 1 41 49 10.1016/0165-0270(83)90050-X 6876872 · DOI
  34. [40]Vaz R Sarmento A Borges N Cruz C Azevedo T Experimental traumatic cerebral contusion: morphological study of brain microvessels and characterization of the oedema Acta Neurochir 1998 140 1 76 81 10.1007/s007010050061 9522912 · DOI
  35. [41]Yen LF Wei VC Kuo EY Lai TW Distinct patterns of cerebral extravasation by Evans blue and sodium fluorescein in rats PLoS ONE 2013 8 7 e68595 10.1371/journal.pone.0068595 23861924 PMC3702610 · DOI
  36. [42]Berger Z Roder H Hanna A Carlson A Rangachari V Yue M Wszolek Z Ashe K Knight J Dickson D Andorfer C Rosenberry TL Lewis J Hutton M Janus C Accumulation of pathological tau species and memory loss in a conditional model of tauopathy J Neurosci 2007 27 14 3650 3662 10.1523/JNEUROSCI.0587-07.2007 17409229 PMC6672413 · DOI
  37. [43]Wes PD Easton A Corradi J Barten DM Devidze N DeCarr LB Truong A He A Barrezueta NX Polson C Bourin C Flynn ME Keenan S Lidge R Meredith J Natale J Sankaranarayanan S Cadelina GW Albright CF Cacace AM Tau overexpression impacts a neuroinflammation gene expression network perturbed in Alzheimer's disease PLoS ONE 2014 9 8 e106050 10.1371/journal.pone.0106050 25153994 PMC4143352 · DOI
  38. [45]Koren J 3rd Jinwal UK Lee DC Jones JR Shults CL Johnson AG Anderson LJ Dickey CA Chaperone signalling complexes in Alzheimer's disease J Cell Mol Med 2009 13 4 619 630 10.1111/j.1582-4934.2008.00557.x 19449461 PMC2749087 · DOI
  39. [46]Imura T Shimohama S Sato M Nishikawa H Madono K Akaike A Kimura J Differential expression of small heat shock proteins in reactive astrocytes after focal ischemia: possible role of beta-adrenergic receptor J Neurosci 1999 19 22 9768 9779 10559386 PMC6782944
  40. [47]Piotrowicz RS Hickey E Levin EG Heat shock protein 27 kDa expression and phosphorylation regulates endothelial cell migration Faseb J 1998 12 14 1481 1490 9806757
  41. [48]Leszczynski D Joenvaara S Reivinen J Kuokka R Non-thermal activation of the hsp27/p38MAPK stress pathway by mobile phone radiation in human endothelial cells: molecular mechanism for cancer- and blood-brain barrier-related effects Differentiation 2002 70 2–3 120 129 10.1046/j.1432-0436.2002.700207.x 12076339 · DOI
  42. [49]San Jose I Garcia-Atares N Pelaez B Cabo R Esteban I Vega JA Represa J Reduction of glial fibrillary acidic protein-immunoreactive astrocytes in some brain areas of old hairless rhino-j mice (hr-rh-j) Neurosci Lett 2001 309 2 81 84 10.1016/S0304-3940(01)02041-9 11502350 · DOI
  43. [50]Schmidt-Kastner R Wietasch K Weigel H Eysel UT Immunohistochemical staining for glial fibrillary acidic protein (GFAP) after deafferentation or ischemic infarction in rat visual system: features of reactive and damaged astrocytes Int J Dev Neurosci 1993 11 2 157 174 10.1016/0736-5748(93)90076-P 7687085 · DOI
  44. [51]Graesser D Solowiej A Bruckner M Osterweil E Juedes A Davis S Ruddle NH Engelhardt B Madri JA Altered vascular permeability and early onset of experimental autoimmune encephalomyelitis in PECAM-1-deficient mice J Clin Invest 2002 109 3 383 392 10.1172/JCI0213595 11827998 PMC150854 · DOI
  45. [52]Choi JJ Wang S Tung YS Morrison B 3rd Konofagou EE Molecules of various pharmacologically-relevant sizes can cross the ultrasound-induced blood-brain barrier opening in vivo Ultrasound Med Biol 2010 36 1 58 67 10.1016/j.ultrasmedbio.2009.08.006 19900750 PMC2997717 · DOI
  46. [53]Pathak AP Kim E Zhang J Jones MV Three-dimensional imaging of the mouse neurovasculature with magnetic resonance microscopy PLoS ONE 2011 6 7 e22643 10.1371/journal.pone.0022643 21818357 PMC3144917 · DOI
  47. [54]Ludvigson AE Luebke JI Lewis J Peters A Structural abnormalities in the cortex of the rTg4510 mouse model of tauopathy: a light and electron microscopy study Brain Struct Funct 2011 216 1 31 42 10.1007/s00429-010-0295-4 21152933 PMC3748379 · DOI
  48. [55]Seiffert E Dreier JP Ivens S Bechmann I Tomkins O Heinemann U Friedman A Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex J Neurosci 2004 24 36 7829 7836 10.1523/JNEUROSCI.1751-04.2004 15356194 PMC6729929 · DOI
  49. [56]Thuringer D Jego G Wettstein G Terrier O Cronier L Yousfi N Hebrard S Bouchot A Hazoume A Joly AL Gleave M Rosa-Calatrava M Solary E Garrido C Extracellular HSP27 mediates angiogenesis through Toll-like receptor 3 Faseb J 2013 27 10 4169 4183 10.1096/fj.12-226977 23804239 · DOI
  50. [57]de Vries HE Kooij G Frenkel D Georgopoulos S Monsonego A Janigro D Inflammatory events at blood-brain barrier in neuroinflammatory and neurodegenerative disorders: implications for clinical disease Epilepsia 2012 53 Suppl 6 45 52 10.1111/j.1528-1167.2012.03702.x 23134495 PMC4853914 · DOI
  51. [58]Merlini M Meyer EP Ulmann-Schuler A Nitsch RM Vascular beta-amyloid and early astrocyte alterations impair cerebrovascular function and cerebral metabolism in transgenic arcAbeta mice Acta Neuropathol 2011 122 3 293 311 10.1007/s00401-011-0834-y 21688176 PMC3168476 · DOI · Paper page
  52. [60]Fiala M Zhang L Gan X Sherry B Taub D Graves MC Hama S Way D Weinand M Witte M Lorton D Kuo YM Roher AE Amyloid-beta induces chemokine secretion and monocyte migration across a human blood–brain barrier model Mol Med 1998 4 7 480 489 9713826 PMC2230332
  53. [62]Lee DC Rizer J Selenica ML Reid P Kraft C Johnson A Blair L Gordon MN Dickey CA Morgan D LPS- induced inflammation exacerbates phospho-tau pathology in rTg4510 mice J Neuroinflammation 2010 7 56 10.1186/1742-2094-7-56 20846376 PMC2949628 · DOI · Paper page
  54. [63]Yamada K Cirrito JR Stewart FR Jiang H Finn MB Holmes BB Binder LI Mandelkow EM Diamond MI Lee VM Holtzman DM In vivo microdialysis reveals age-dependent decrease of brain interstitial fluid tau levels in P301S human tau transgenic mice J Neurosci 2011 31 37 13110 13117 10.1523/JNEUROSCI.2569-11.2011 21917794 PMC4299126 · DOI · Paper page
  55. [64]Yamada K Holth JK Liao F Stewart FR Mahan TE Jiang H Cirrito JR Patel TK Hochgrafe K Mandelkow EM Holtzman DM Neuronal activity regulates extracellular tau in vivo J Exp Med 2014 211 3 387 393 10.1084/jem.20131685 24534188 PMC3949564 · DOI
  56. [66]Hall GF Patuto BA Is tau ready for admission to the prion club? Prion 2012 6 3 223 233 10.4161/pri.19912 22561167 PMC3399531 · DOI
  57. [67]Iba M Guo JL McBride JD Zhang B Trojanowski JQ Lee VM Synthetic tau fibrils mediate transmission of neurofibrillary tangles in a transgenic mouse model of Alzheimer's-like tauopathy J Neurosci 2013 33 3 1024 1037 10.1523/JNEUROSCI.2642-12.2013 23325240 PMC3575082 · DOI · Paper page
  58. [68]Lasagna-Reeves CA Sengupta U Castillo-Carranza D Gerson JE Guerrero-Munoz M Troncoso JC Jackson GR Kayed R The formation of tau pore-like structures is prevalent and cell specific: possible implications for the disease phenotypes Acta Neuropathol Commun 2014 2 1 56 10.1186/2051-5960-2-56 24887264 PMC4231072 · DOI
  59. [69]Lasagna-Reeves CA Castillo-Carranza DL Sengupta U Sarmiento J Troncoso J Jackson GR Kayed R Identification of oligomers at early stages of tau aggregation in Alzheimer's disease Faseb J 2012 26 5 1946 1959 10.1096/fj.11-199851 22253473 PMC4046102 · DOI · Paper page
  60. [70]Ochoa CD Alexeyev M Pastukh V Balczon R Stevens T Pseudomonas aeruginosa exotoxin Y is a promiscuous cyclase that increases endothelial tau phosphorylation and permeability J Biol Chem 2012 287 30 25407 25418 10.1074/jbc.M111.301440 22637478 PMC3408204 · DOI
  61. [71]Zhu B Zhang L Creighton J Alexeyev M Strada SJ Stevens T Protein kinase A phosphorylation of tau-serine 214 reorganizes microtubules and disrupts the endothelial cell barrier Am J Physiol Lung Cell Mol Physiol 2010 299 4 L493 L501 10.1152/ajplung.00431.2009 20639351 PMC2957413 · DOI
  62. [72]Birukova AA Birukov KG Smurova K Adyshev D Kaibuchi K Alieva I Garcia JG Verin AD Novel role of microtubules in thrombin-induced endothelial barrier dysfunction Faseb J 2004 18 15 1879 1890 10.1096/fj.04-2328com 15576491 · DOI
  63. [73]Ghetti B Piccardo P Spillantini MG Ichimiya Y Porro M Perini F Kitamoto T Tateishi J Seiler C Frangione B Bugiani O Giaccone G Prelli F Goedert M Dlouhy SR Tagliavini F Vascular variant of prion protein cerebral amyloidosis with tau-positive neurofibrillary tangles: the phenotype of the stop codon 145 mutation in PRNP Proc Natl Acad Sci U S A 1996 93 2 744 748 10.1073/pnas.93.2.744 8570627 PMC40125 · DOI
  64. [74]Williams S Chalmers K Wilcock GK Love S Relationship of neurofibrillary pathology to cerebral amyloid angiopathy in Alzheimer's disease Neuropathol Appl Neurobiol 2005 31 4 414 421 10.1111/j.1365-2990.2005.00663.x 16008825 · DOI · Paper page
  65. [75]Sagare AP Bell RD Zlokovic BV Neurovascular defects and faulty amyloid-beta vascular clearance in Alzheimer's disease J Alzheimers Dis 2013 33 Suppl 1 S87 S100 22751174 PMC4416477
  66. [76]Dickson DW Neuropathologic differentiation of progressive supranuclear palsy and corticobasal degeneration J Neurol 1999 246 Suppl 2 II6 II15 10.1007/BF03161076 10525997 · DOI
  67. [77]van Assema DM Lubberink M Rizzu P van Swieten JC Schuit RC Eriksson J Scheltens P Koepp M Lammertsma AA van Berckel BN Blood-brain barrier P-glycoprotein function in healthy subjects and Alzheimer's disease patients: effect of polymorphisms in the ABCB1 gene EJNMMI Res 2012 2 1 57 10.1186/2191-219X-2-57 23067778 PMC3483228 · DOI
  68. [79]Forman MS Zhukareva V Bergeron C Chin SS Grossman M Clark C Lee VM Trojanowski JQ Signature tau neuropathology in gray and white matter of corticobasal degeneration Am J Pathol 2002 160 6 2045 2053 10.1016/S0002-9440(10)61154-6 12057909 PMC1850831 · DOI
  69. [80]Ikeda K Akiyama H Kondo H Haga C Tanno E Tokuda T Ikeda S Thorn-shaped astrocytes: possibly secondarily induced tau-positive glial fibrillary tangles Acta Neuropathol 1995 90 6 620 625 10.1007/BF00318575 8615083 · DOI · Paper page
  70. [81]Shibuya K Yagishita S Nakamura A Uchihara T Perivascular orientation of astrocytic plaques and tuft-shaped astrocytes Brain Res 2011 1404 50 54 10.1016/j.brainres.2011.06.014 21722877 · DOI
  71. [82]Brochard V Combadiere B Prigent A Laouar Y Perrin A Beray-Berthat V Bonduelle O Alvarez-Fischer D Callebert J Launay JM Duyckaerts C Flavell RA Hirsch EC Hunot S Infiltration of CD4+ lymphocytes into the brain contributes to neurodegeneration in a mouse model of Parkinson disease J Clin Invest 2009 119 1 182 192 19104149 PMC2613467
  72. [83]Mandrekar-Colucci S Landreth GE Microglia and inflammation in Alzheimer's disease CNS Neurol Disord Drug Targets 2010 9 2 156 167 10.2174/187152710791012071 20205644 PMC3653290 · DOI · Paper page
  73. [84]McGeer PL McGeer EG Inflammation and the degenerative diseases of aging Ann N Y Acad Sci 2004 1035 104 116 10.1196/annals.1332.007 15681803 · DOI
  74. [85]Rogers J Luber-Narod J Styren SD Civin WH Expression of immune system-associated antigens by cells of the human central nervous system: relationship to the pathology of Alzheimer's disease Neurobiol Aging 1988 9 4 339 349 10.1016/S0197-4580(88)80079-4 3263583 · DOI · Paper page

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Authors
Blair, L. J., Frauen, H. D., Zhang, B., Nordhues, B. A., Bijan, S., Lin, Y.-C., Zamudio, F., Hernandez, L. D., Sabbagh, J. J., Selenica, M.-L. B., & Dickey, C. A.
Affiliations
University of South Florida (US)
Corresponding author
Dickey, Chad A
ORCID
Venue
Acta Neuropathologica Communications
Publisher
Springer Science and Business Media LLC
Published
2015-01-31
Volume
3
Issue
1
Pages
8-8
ISSN
2051-5960 (ISSN-L)
DOI
10.1186/s40478-015-0186-2
PMC
PMC4353464
OpenAlex
W2154271806
Cited by
193
References
11
Citations by year
2026: 8 · 2025: 26 · 2024: 27 · 2023: 16 · 2022: 14 · 2021: 17 · 2020: 26 · 2019: 17 · 2018: 13 · 2017: 9 · 2016: 10 · 2015: 9 · 2012: 1
FWCI
7.30
Type
journal article
Language
en
Open access
Licence
Locations
  • Acta Neuropathologica Communications (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • U.S. Department of Veterans Affairs (BX001637, I01 BX001637)
  • National Institutes of Health
  • James A. Haley Veterans' Hospital (BX001637)
  • National Institute of Neurological Disorders and Stroke (R01NS073899)
Topics
  • Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
  • Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
Keywords
tauopathy, blood-brain barrier, progressive supranuclear palsy, Alzheimer's disease, blood-brain barrier permeability, neuroinflammation, brain atrophy, doxycycline, vascular dementia, cognitive impairment
MeSH terms
Age Factors, Analysis of Variance, Animals, Blood-Brain Barrier, Disease Models, Animal, Doxycycline, Erythrocytes, Gene Expression Regulation, Glial Fibrillary Acidic Protein, Hippocampus, Immunoglobulin G, Longitudinal Studies, Mice, Transgenic, T-Lymphocytes, Antigens, CD, tau Proteins, Disease Progression, Tauopathies, Mice, HSP27 Heat-Shock Proteins

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