CoChat
Sign Up
Cited by 53Traumatic Brain Injury and Neurovascular DisturbancesTraumatic Brain Injury ResearchAlzheimer's disease research and treatments

Mouse closed head traumatic brain injury replicates the histological tau pathology pattern of human disease: Characterization of a novel model and systematic review of the literature

Open access
Kahriman, Aydan, Bouley, James, Smith, Thomas W., Bosco, Daryl A., Woerman, Amanda L., Henninger, Nils·2021·Acta Neuropathologica Communications
DOI 10.1186/s40478-021-01220-8PMC PMC8243463
Open this paper in CoChat — free accountOpen PDF

Abstract

Traumatic brain injury (TBI) constitutes one of the strongest environmental risk factors for several progressive neurodegenerative disorders of cognitive impairment and dementia that are characterized by the pathological accumulation of hyperphosphorylated tau (p-Tau). It has been questioned whether mouse closed-head TBI models can replicate human TBI-associated tauopathy. We conducted longitudinal histopathological characterization of a mouse closed head TBI model, with a focus on pathological features reported in human TBI-associated tauopathy. Male C57BL/6 J mice were subjected to once daily TBI for 5 consecutive days using a weight drop paradigm. Histological analyses (AT8, TDP-43, pTDP-43, NeuN, GFAP, Iba-1, MBP, SMI-312, Prussian blue, IgG, βAPP, alpha-synuclein) were conducted at 1 week, 4 weeks, and 24 weeks after rTBI and compared to sham operated controls. We conducted a systematic review of the literature for mouse models of closed-head injury focusing on studies referencing tau protein assessment. At 1-week post rTBI, p-Tau accumulation was restricted to the corpus callosum and perivascular spaces adjacent to the superior longitudinal fissure. Progressive p-Tau accumulation was observed in the superficial layers of the cerebral cortex, as well as in mammillary bodies and cortical perivascular, subpial, and periventricular locations at 4 to 24 weeks after rTBI. Associated cortical histopathologies included microvascular injury, neuroaxonal rarefaction, astroglial and microglial activation, and cytoplasmatic localization of TDP-43 and pTDP-43. In our systematic review, less than 1% of mouse studies (25/3756) reported p-Tau using immunostaining, of which only 3 (0.08%) reported perivascular p-Tau, which is considered a defining feature of chronic traumatic encephalopathy. Commonly reported associated pathologies included neuronal loss (23%), axonal loss (43%), microglial activation and astrogliosis (50%, each), and beta amyloid deposition (29%). Our novel model, supported by systematic review of the literature, indicates progressive tau pathology after closed head murine TBI, highlighting the suitability of mouse models to replicate pertinent human histopathology.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1186/s40478-021-01220-8

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 72

  1. [1]Albayram O Kondo A Mannix R Smith C Tsai CY Li C Herbert MK Qiu J Monuteaux M Driver J Cis P-tau is induced in clinical and preclinical brain injury and contributes to post-injury sequelae Nat Commun 2017 8 1000 10.1038/s41467-017-01068-4 29042562 PMC5645414 · DOI
  2. [2]Albayram O MacIver B Mathai J Verstegen A Baxley S Qiu C Bell C Caldarone BJ Zhou XZ Lu KP Traumatic Brain Injury-related voiding dysfunction in mice is caused by damage to rostral pathways, altering inputs to the reflex pathways Sci Rep 2019 9 8646 10.1038/s41598-019-45234-8 31201348 PMC6570649 · DOI
  3. [3]Angoa-Perez M Zagorac B Anneken JH Briggs DI Winters AD Greenberg JM Ahmad M Theis KR Kuhn DM Repetitive, mild traumatic brain injury results in a progressive white matter pathology, cognitive deterioration, and a transient gut microbiota dysbiosis Sci Rep 2020 10 8949 10.1038/s41598-020-65972-4 32488168 PMC7265445 · DOI
  4. [4]Anonymous (1999) Consensus conference. Rehabilitation of persons with traumatic brain injury. NIH consensus development panel on rehabilitation of persons with traumatic brain injury. JAMA 282: 974-983 10485684
  5. [5]Arena JD Smith DH Lee EB Gibbons GS Irwin DJ Robinson JL Lee VM Trojanowski JQ Stewart W Johnson VE Tau immunophenotypes in chronic traumatic encephalopathy recapitulate those of ageing and Alzheimer's disease Brain 2020 143 1572 1587 10.1093/brain/awaa071 32390044 PMC7241956 · DOI
  6. [7]Baugh CM Stamm JM Riley DO Gavett BE Shenton ME Lin A Nowinski CJ Cantu RC McKee AC Stern RA Chronic traumatic encephalopathy: neurodegeneration following repetitive concussive and subconcussive brain trauma Brain Imaging Behav 2012 6 244 254 10.1007/s11682-012-9164-5 22552850 · DOI · Paper page
  7. [8]Bieniek KF Cairns NJ Crary JF Dickson DW Folkerth RD Keene CD Litvan I Perl DP Stein TD Vonsattel JP The second NINDS/NIBIB consensus meeting to define neuropathological criteria for the diagnosis of chronic traumatic encephalopathy J Neuropathol Exp Neurol 2021 80 210 219 10.1093/jnen/nlab001 33611507 PMC7899277 · DOI
  8. [9]Bodnar CN Roberts KN Higgins EK Bachstetter AD A systematic review of closed head injury models of mild traumatic brain injury in mice and rats J Neurotrauma 2019 36 1683 1706 10.1089/neu.2018.6127 30661454 PMC6555186 · DOI
  9. [10]Bolton-Hall AN Hubbard WB Saatman KE Experimental designs for repeated mild traumatic brain injury: challenges and considerations J Neurotrauma 2019 36 1203 1221 10.1089/neu.2018.6096 30351225 PMC6479246 · DOI
  10. [11]Bouley J Chung DY Ayata C Brown RH Jr Henninger N Cortical spreading depression denotes concussion injury J Neurotrauma 2019 36 1008 1017 10.1089/neu.2018.5844 29999455 PMC6444888 · DOI
  11. [12]Bradshaw DR Ivarsson J Morfey CL Viano DC Simulation of acute subdural hematoma and diffuse axonal injury in coronal head impact J Biomech 2001 34 85 94 10.1016/s0021-9290(00)00135-4 11425084 · DOI
  12. [13]Briggs DI Angoa-Perez M Kuhn DM Prolonged repetitive head trauma induces a singular chronic traumatic encephalopathy-like pathology in white matter despite transient behavioral abnormalities Am J Pathol 2016 186 2869 2886 10.1016/j.ajpath.2016.07.013 27662795 · DOI
  13. [14]Cansler SM, Guilhaume-Correa F, Day D, Bedolla A, Evanson NK Indirect traumatic optic neuropathy after head trauma in adolescent male mice is associated with behavioral visual impairment, neurodegeneration, and elevated endoplasmic reticulum stress markers at acute and subacute times. BioRxiv [Preprint] June 12, 2020 (Cited 06/01/2021). 10.1101/2020.06.11.144766 · DOI
  14. [15]Cheng WH Martens KM Bashir A Cheung H Stukas S Gibbs E Namjoshi DR Button EB Wilkinson A Barron CJ CHIMERA repetitive mild traumatic brain injury induces chronic behavioural and neuropathological phenotypes in wild-type and APP/PS1 mice Alzheimers Res Ther 2019 11 6 10.1186/s13195-018-0461-0 30636629 PMC6330571 · DOI
  15. [16]Cloots RJ Gervaise HM van Dommelen JA Geers MG Biomechanics of traumatic brain injury: influences of the morphologic heterogeneities of the cerebral cortex Ann Biomed Eng 2008 36 1203 1215 10.1007/s10439-008-9510-3 18465248 PMC2413127 · DOI · Paper page
  16. [17]Crane PK Gibbons LE Dams-O'Connor K Trittschuh E Leverenz JB Keene CD Sonnen J Montine TJ Bennett DA Leurgans S Association of traumatic brain injury with late-life neurodegenerative conditions and neuropathologic findings JAMA Neurol 2016 73 1062 1069 10.1001/jamaneurol.2016.1948 27400367 PMC5319642 · DOI
  17. [18]DeWitt DS Hawkins BE Dixon CE Kochanek PM Armstead W Bass CR Bramlett HM Buki A Dietrich WD Ferguson AR Pre-clinical testing of therapies for traumatic brain injury J Neurotrauma 2018 35 2737 2754 10.1089/neu.2018.5778 29756522 PMC8349722 · DOI
  18. [19]Evanson NK Guilhaume-Correa F Herman JP Goodman MD Optic tract injury after closed head traumatic brain injury in mice: A model of indirect traumatic optic neuropathy PLoS ONE 2018 13 e0197346 10.1371/journal.pone.0197346 29746557 PMC5944994 · DOI
  19. [20]Fleminger S Ponsford J Long term outcome after traumatic brain injury BMJ 2005 331 1419 1420 10.1136/bmj.331.7530.1419 16356951 PMC1315633 · DOI
  20. [21]Gamache J Benzow K Forster C Kemper L Hlynialuk C Furrow E Ashe KH Koob MD Factors other than hTau overexpression that contribute to tauopathy-like phenotype in rTg4510 mice Nat Commun 2019 10 2479 10.1038/s41467-019-10428-1 31171783 PMC6554306 · DOI
  21. [22]Gavett BE Stern RA McKee AC Chronic traumatic encephalopathy: a potential late effect of sport-related concussive and subconcussive head trauma Clin Sports Med 2011 30 179 188 10.1016/j.csm.2010.09.007 21074091 PMC2995699 · DOI · Paper page
  22. [23]Ghajari M Hellyer PJ Sharp DJ Computational modelling of traumatic brain injury predicts the location of chronic traumatic encephalopathy pathology Brain 2017 140 333 343 10.1093/brain/aww317 28043957 PMC5278309 · DOI
  23. [24]Goedert M Eisenberg DS Crowther RA Propagation of tau aggregates and neurodegeneration Annu Rev Neurosci 2017 40 189 210 10.1146/annurev-neuro-072116-031153 28772101 · DOI · Paper page
  24. [26]Goldstein LE Fisher AM Tagge CA Zhang XL Velisek L Sullivan JA Upreti C Kracht JM Ericsson M Wojnarowicz MW Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model Sci Transl Med 2012 4 134 160 10.1126/scitranslmed.3003716 PMC3739428 22593173 · DOI · Paper page
  25. [27]Graham NS Sharp DJ Understanding neurodegeneration after traumatic brain injury: from mechanisms to clinical trials in dementia J Neurol Neurosurg Psychiatry 2019 90 1221 1233 10.1136/jnnp-2017-317557 31542723 PMC6860906 · DOI
  26. [28]Griffin AD Turtzo LC Parikh GY Tolpygo A Lodato Z Moses AD Nair G Perl DP Edwards NA Dardzinski BJ Traumatic microbleeds suggest vascular injury and predict disability in traumatic brain injury Brain 2019 142 3550 3564 10.1093/brain/awz290 31608359 PMC6821371 · DOI
  27. [29]Guo Z Cupples LA Kurz A Auerbach SH Volicer L Chui H Green RC Sadovnick AD Duara R DeCarli C Head injury and the risk of AD in the MIRAGE study Neurology 2000 54 1316 1323 10.1212/wnl.54.6.1316 10746604 · DOI · Paper page
  28. [30]Gyparaki MT Arab A Sorokina EM Santiago-Ruiz AN Bohrer CH Xiao J Lakadamyali M Tau forms oligomeric complexes on microtubules that are distinct from tau aggregates Proc Natl Acad Sci U S A 2021 10.1073/pnas.2021461118 33952699 PMC8126857 · DOI
  29. [31]Henninger N Bouley J Sikoglu EM An J Moore CM King JA Bowser R Freeman MR Brown RH Jr Attenuated traumatic axonal injury and improved functional outcome after traumatic brain injury in mice lacking Sarm1 Brain 2016 139 1094 1105 10.1093/brain/aww001 26912636 PMC5006226 · DOI
  30. [32]Hernandez F Merchan-Rubira J Valles-Saiz L Rodriguez-Matellan A Avila J Differences between human and murine tau at the N-terminal end Front Aging Neurosci 2020 12 11 10.3389/fnagi.2020.00011 32063841 PMC6999090 · DOI
  31. [33]Holtzman DM Carrillo MC Hendrix JA Bain LJ Catafau AM Gault LM Goedert M Mandelkow E Mandelkow EM Miller DS Tau: From research to clinical development Alzheimers Dement 2016 12 1033 1039 10.1016/j.jalz.2016.03.018 27154059 · DOI · Paper page
  32. [34]Hsu ET Gangolli M Su S Holleran L Stein TD Alvarez VE McKee AC Schmidt RE Brody DL Astrocytic degeneration in chronic traumatic encephalopathy Acta Neuropathol 2018 136 955 972 10.1007/s00401-018-1902-3 30194648 · DOI
  33. [35]Huber BR Meabon JS Martin TJ Mourad PD Bennett R Kraemer BC Cernak I Petrie EC Emery MJ Swenson ER Blast exposure causes early and persistent aberrant phospho- and cleaved-tau expression in a murine model of mild blast-induced traumatic brain injury J Alzheimers Dis 2013 37 309 323 10.3233/JAD-130182 23948882 PMC4126588 · DOI
  34. [36]Hyder AA Wunderlich CA Puvanachandra P Gururaj G Kobusingye OC The impact of traumatic brain injuries: a global perspective NeuroRehabilitation 2007 22 341 353 10.3233/NRE-2007-22502 18162698 · DOI · Paper page
  35. [37]Iliff JJ Chen MJ Plog BA Zeppenfeld DM Soltero M Yang L Singh I Deane R Nedergaard M Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury J Neurosci 2014 34 16180 16193 10.1523/JNEUROSCI.3020-14.2014 25471560 PMC4252540 · DOI · Paper page
  36. [39]Kenney K Amyot F Haber M Pronger A Bogoslovsky T Moore C Diaz-Arrastia R Cerebral vascular injury in traumatic brain injury Exp Neurol 2016 275 Pt 3 353 366 10.1016/j.expneurol.2015.05.019 26048614 · DOI
  37. [40]Kondo A Shahpasand K Mannix R Qiu J Moncaster J Chen CH Yao Y Lin YM Driver JA Sun Y Antibody against early driver of neurodegeneration cis P-tau blocks brain injury and tauopathy Nature 2015 523 431 436 10.1038/nature14658 26176913 PMC4718588 · DOI · Paper page
  38. [41]Kovacs GG Astroglia and Tau: new perspectives Front Aging Neurosci 2020 12 96 10.3389/fnagi.2020.00096 32327993 PMC7160822 · DOI · Paper page
  39. [42]Liu B Cao Y Shi F Wang L Li N Cheng X Du J Tian Q Zhou X The overexpression of RBM3 alleviates TBI-induced behaviour impairment and AD-like tauopathy in mice J Cell Mol Med 2020 24 9176 9188 10.1111/jcmm.15555 32648620 PMC7417709 · DOI
  40. [43]Logsdon AF Lucke-Wold BP Turner RC Li X Adkins CE Mohammad AS Huber JD Rosen CL Lockman PR A mouse model of focal vascular injury induces astrocyte reactivity, tau oligomers, and aberrant behavior Arch Neurosci 2017 10.5812/archneurosci.44254 28758136 PMC5529099 · DOI
  41. [44]Luo J Nguyen A Villeda S Zhang H Ding Z Lindsey D Bieri G Castellano JM Beaupre GS Wyss-Coray T Long-term cognitive impairments and pathological alterations in a mouse model of repetitive mild traumatic brain injury Front Neurol 2014 5 12 10.3389/fneur.2014.00012 24550885 PMC3912443 · DOI
  42. [45]McKee AC Abdolmohammadi B Stein TD The neuropathology of chronic traumatic encephalopathy Handb Clin Neurol 2018 158 297 307 10.1016/B978-0-444-63954-7.00028-8 30482357 · DOI
  43. [47]McKee AC Gavett BE Stern RA Nowinski CJ Cantu RC Kowall NW Perl DP Hedley-Whyte ET Price B Sullivan C TDP-43 proteinopathy and motor neuron disease in chronic traumatic encephalopathy J Neuropathol Exp Neurol 2010 69 918 929 10.1097/NEN.0b013e3181ee7d85 20720505 PMC2951281 · DOI · Paper page
  44. [48]McKee AC Robinson ME Military-related traumatic brain injury and neurodegeneration Alzheimers Dement 2014 10 S242 253 10.1016/j.jalz.2014.04.003 24924675 PMC4255273 · DOI · Paper page
  45. [50]Niziolek GM Boudreau RM Baker J Friend LA Makley AT Edwards MJ Gulbins E Goodman MD Acid sphingomyelinase inhibition mitigates histopathological and behavioral changes in a murine model of traumatic brain injury J Neurotrauma 2020 37 1902 1909 10.1089/neu.2019.6436 32138594 PMC7484895 · DOI
  46. [51]Niziolek GM Hoehn RS Seitz AP Jernigan PL Makley AT Gulbins E Edwards MJ Goodman MD The role of acid sphingomyelinase inhibition in repetitive mild traumatic brain injury J Surg Res 2021 259 296 304 10.1016/j.jss.2020.09.034 33131764 PMC7897232 · DOI
  47. [52]Paxinos G Franklin KBJ The mouse brain in stereotaxic coordinates 2013 Cambridge Elsevier Academic Press
  48. [53]Peeters W van den Brande R Polinder S Brazinova A Steyerberg EW Lingsma HF Maas AI Epidemiology of traumatic brain injury in Europe Acta Neurochir (Wien) 2015 157 1683 1696 10.1007/s00701-015-2512-7 26269030 PMC4569652 · DOI
  49. [54]Petraglia AL Plog BA Dayawansa S Dashnaw ML Czerniecka K Walker CT Chen M Hyrien O Iliff JJ Deane R The pathophysiology underlying repetitive mild traumatic brain injury in a novel mouse model of chronic traumatic encephalopathy Surg Neurol Int 2014 5 184 10.4103/2152-7806.147566 25593768 PMC4287910 · DOI · Paper page
  50. [55]Rajic Bumber J Pilipovic K Jankovic T Dolenec P Grzeta N Kriz J Zupan G Repetitive traumatic brain injury is associated with TDP-43 alterations, neurodegeneration, and glial activation in mice J Neuropathol Exp Neurol 2021 80 2 14 10.1093/jnen/nlaa130 33212475 · DOI
  51. [56]Rehman SU Ahmad A Yoon GH Khan M Abid MN Kim MO Inhibition of c-Jun N-terminal kinase protects against brain damage and improves learning and memory after traumatic brain injury in adult mice Cereb Cortex 2018 28 2854 2872 10.1093/cercor/bhx164 29088310 · DOI
  52. [57]Sabbagh JJ Fontaine SN Shelton LB Blair LJ Hunt JB Jr Zhang B Gutmann JM Lee DC Lloyd JD Dickey CA Noncontact rotational head injury produces transient cognitive deficits but lasting neuropathological changes J Neurotrauma 2016 33 1751 1760 10.1089/neu.2015.4288 26739819 PMC5065038 · DOI
  53. [58]Sacramento CB Sondhi D Rosenberg JB Chen A Giordano S Pey E Lee V Stiles KM Havlicek DF Leopold PL Anti-phospho-tau gene therapy for chronic traumatic encephalopathy Hum Gene Ther 2020 31 57 69 10.1089/hum.2019.174 31608704 · DOI
  54. [59]Santacruz K Lewis J Spires T Paulson J Kotilinek L Ingelsson M Guimaraes A DeTure M Ramsden M McGowan E Tau suppression in a neurodegenerative mouse model improves memory function Science 2005 309 476 481 10.1126/science.1113694 16020737 PMC1574647 · DOI · Paper page
  55. [60]Schneider CA Rasband WS Eliceiri KW NIH Image to ImageJ: 25 years of image analysis Nat Methods 2012 9 671 675 10.1038/nmeth.2089 22930834 PMC5554542 · DOI · Paper page
  56. [61]Schneider J, Jeon S, Gladman JT, Corriveau RA ADRD Summit 2019 Report to the National Advisory Neurological Disorders and Stroke Council. https://www.ninds.nih.gov/News-Events/Events-Proceedings/Events/Alzheimers-Disease-Related-Dementias-Summit-2019 accessed 05/13/2020
  57. [62]Selvaraj P Wen J Tanaka M Zhang Y Therapeutic effect of a novel fatty acid amide hydrolase inhibitor PF04457845 in the repetitive closed head injury mouse model J Neurotrauma 2019 36 1655 1669 10.1089/neu.2018.6226 30526351 · DOI
  58. [63]Seo JS Lee S Shin JY Hwang YJ Cho H Yoo SK Kim Y Lim S Kim YK Hwang EM Transcriptome analyses of chronic traumatic encephalopathy show alterations in protein phosphatase expression associated with tauopathy Exp Mol Med 2017 49 e333 10.1038/emm.2017.56 28524178 PMC5454448 · DOI
  59. [64]Shin N Kim HG Shin HJ Kim S Kwon HH Baek H Yi MH Zhang E Kim JJ Hong J Uncoupled endothelial nitric oxide synthase enhances p-Tau in chronic traumatic encephalopathy mouse model Antioxid Redox Signal 2019 30 1601 1620 10.1089/ars.2017.7280 30070145 · DOI
  60. [65]Sidoryk-Wegrzynowicz M Struzynska L Astroglial contribution to tau-dependent neurodegeneration Biochem J 2019 476 3493 3504 10.1042/BCJ20190506 31774919 · DOI
  61. [66]Smith DH Dolle JP Ameen-Ali KE Bretzin A Cortes E Crary JF Dams-O'Connor K Diaz-Arrastia R Edlow BL Folkerth R Collaborative neuropathology network characterizing outcomes of TBI (CONNECT-TBI) Acta Neuropathol Commun 2021 9 32 10.1186/s40478-021-01122-9 33648593 PMC7919306 · DOI
  62. [67]Smith DH Johnson VE Stewart W Chronic neuropathologies of single and repetitive TBI: substrates of dementia? Nat Rev Neurol 2013 9 211 221 10.1038/nrneurol.2013.29 23458973 PMC4513655 · DOI · Paper page
  63. [68]Smith VD Bachstetter AD Ighodaro E Roberts K Abner EL Fardo DW Nelson PT Overlapping but distinct TDP-43 and tau pathologic patterns in aged hippocampi Brain Pathol 2018 28 264 273 10.1111/bpa.12505 28281308 PMC5591757 · DOI
  64. [69]Tagge CA Fisher AM Minaeva OV Gaudreau-Balderrama A Moncaster JA Zhang XL Wojnarowicz MW Casey N Lu H Kokiko-Cochran ON Concussion, microvascular injury, and early tauopathy in young athletes after impact head injury and an impact concussion mouse model Brain 2018 141 422 458 10.1093/brain/awx350 29360998 PMC5837414 · DOI
  65. [70]Tan XL Sun M Brady RD Liu S Llanos R Cheung S Wright DK Casillas-Espinosa PM Sashindranath M O'Brien TJ Transactive Response DNA-Binding Protein 43 Abnormalities after Traumatic Brain Injury J Neurotrauma. 2019 36 87 99 10.1089/neu.2017.5491 29901412 · DOI
  66. [71]Tang SJ Fesharaki-Zadeh A Takahashi H Nies SH Smith LM Luo A Chyung A Chiasseu M Strittmatter SM Fyn kinase inhibition reduces protein aggregation, increases synapse density and improves memory in transgenic and traumatic Tauopathy Acta Neuropathol Commun 2020 8 96 10.1186/s40478-020-00976-9 32611392 PMC7329553 · DOI
  67. [72]Thau-Zuchman O Shohami E Alexandrovich AG Trembovler V Leker RR The anti-inflammatory drug carprofen improves long-term outcome and induces gliogenesis after traumatic brain injury J Neurotrauma 2012 29 375 384 10.1089/neu.2010.1673 21561314 · DOI
  68. [73]Wiesner D Tar L Linkus B Chandrasekar A Olde Heuvel F Dupuis L Tsao W Wong PC Ludolph A Roselli F Reversible induction of TDP-43 granules in cortical neurons after traumatic injury Exp Neurol 2018 299 15 25 10.1016/j.expneurol.2017.09.011 28941811 · DOI
  69. [74]Woerman AL Patel S Kazmi SA Oehler A Freyman Y Espiritu L Cotter R Castaneda JA Olson SH Prusiner SB Kinetics of human mutant tau prion formation in the brains of 2 transgenic mouse lines JAMA Neurol 2017 74 1464 1472 10.1001/jamaneurol.2017.2822 29059326 PMC5822201 · DOI · Paper page
  70. [75]Xu X Cowan M Beraldo F Schranz A McCunn P Geremia N Brown Z Patel M Nygard KL Khazaee R Repetitive mild traumatic brain injury in mice triggers a slowly developing cascade of long-term and persistent behavioral deficits and pathological changes Acta Neuropathol Commun 2021 9 60 10.1186/s40478-021-01161-2 33823944 PMC8025516 · DOI
  71. [76]Yang Z Wang P Morgan D Lin D Pan J Lin F Strang KH Selig TM Perez PD Febo M Temporal MRI characterization, neurobiochemical and neurobehavioral changes in a mouse repetitive concussive head injury model Sci Rep 2015 5 11178 10.1038/srep11178 26058556 PMC4461921 · DOI
  72. [78]Zhang J Teng Z Song Y Hu M Chen C Inhibition of monoacylglycerol lipase prevents chronic traumatic encephalopathy-like neuropathology in a mouse model of repetitive mild closed head injury J Cereb Blood Flow Metab 2015 35 706 10.1038/jcbfm.2014.247 25826320 PMC4420888 · DOI

Cited by

Sorted by citations

Authors
Kahriman, A., Bouley, J., Smith, T. W., Bosco, D. A., Woerman, A. L., & Henninger, N.
Affiliations
  • University of Massachusetts Chan Medical School (US)
  • University of Massachusetts Amherst (US)
Corresponding author
Henninger, Nils
ORCID
Venue
Acta Neuropathologica Communications
Publisher
Springer Science and Business Media LLC
Published
2021-06-29
Volume
9
Issue
1
Pages
118-118
ISSN
2051-5960 (ISSN-L)
DOI
10.1186/s40478-021-01220-8
PMC
PMC8243463
OpenAlex
W3176711716
Cited by
53
References
6
Citations by year
2026: 5 · 2025: 14 · 2024: 12 · 2023: 10 · 2022: 9 · 2021: 3
FWCI
1.09
Type
journal article
Language
en
Open access
Licence
Locations
  • Acta Neuropathologica Communications (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
National Institute of Neurological Disorders and Stroke (K08NS091499)
Topics
  • Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
  • Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Keywords
traumatic brain injury, closed head injury, tau hyperphosphorylation, tauopathy, mouse model, weight-drop injury, chronic traumatic encephalopathy, TDP-43, neurodegeneration, microglial activation, astrocyte activation, axonal loss, amyloid-beta
MeSH terms
Chronic Traumatic Encephalopathy, Brain Injuries, Traumatic, Animals, Disease Models, Animal, Humans, Male, Mice, Inbred C57BL, Head Injuries, Closed, Tauopathies, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review