Cited by 133Alzheimer's disease research and treatmentsTraumatic Brain Injury ResearchTraumatic Brain Injury and Neurovascular Disturbances

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Enhanced Neurofibrillary Tangle Formation, Cerebral Atrophy, and Cognitive Deficits Induced by Repetitive Mild Brain Injury in a Transgenic Tauopathy Mouse Model

Yoshiyama, Yasumasa, Uryu, Kunihiro, Higuchi, Makoto, Longhi, Luca, Hoover, Rachel, Fujimoto, Scott, McIntosh, Tracy, Lee, Virginia M.-Y., Trojanowski, John Q.·2005·Journal of Neurotrauma

DOI 10.1089/neu.2005.22.1134

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Abstract

Traumatic brain injury (TBI) is a risk factors for Alzheimer's disease (AD), and repetitive TBI (rTBI) may culminate in dementia pugilistica (DP), a syndrome characterized by progressive dementia, parkinsonism, and the hallmark brain lesions of AD, including neurofibrillary tangles (NFTs), formed by abnormal tau filaments and senile plaques (SPs) composed of Abeta fibrils. Previous study showed that mild rTBI (mrTBI) accelerated the deposition of Abeta in the brains of transgenic (Tg) mice (Tg2576) that over-express human Abeta precursor proteins with the familial AD Swedish mutations (APP695swe) and model of AD-like amyloidosis. Here, we report studies of the effects of mrTBI on AD-like tau pathologies in Tg mice expressing the shortest human tau isoform (T44) subjected to mrTBI, causing brain concussion without structural brain damage to simulate injuries linked to DP. Twelve-month-old Tg T44 (n = 18) and wild-type (WT; n = 24) mice were subjected to mrTBI (four times a day, 1 day per week, for 4 weeks; n = 24) or sham treatment (n = 18). Histopathological analysis of mice at 9 months after mrTBI revealed that one of the Tg T44 mice showed extensive telencephalic NFT and cerebral atrophy. Although statistical analysis of neurobehavioral tests at 6 months after mrTBI did not show any significant difference in any of groups of mice, the Tg T44 mouse with extensive NFT had an exceptionally low neurobehavioral score. The reasons for the augmentation of tau pathologies in only o…

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Place navigation impaired in rats with hippocampal lesions
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Self-citation
Tau immunohistochemistry in acute brain injury
Smith, C., Graham, D. I., Murray, L. S., & Nicoll, J. A. R. (2003) · Neuropathology and Applied Neurobiology · doi:10.1046/j.1365-2990.2003.00488.x · Cited by 110 · cited 1×
“…clinically by a progressive dementia with parkinsonism, as well as postmortem evidence of abundant senile plaques (SPs) formed by A deposits and neurofibrillary tangles (NFTs) composed of abnormal tau filaments similar to AD (Geddes et al., 1996; Schmidt et al., 2001; Smith et al., 2003).”

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“[19–22].”
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Result
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Background
Inhibition of Monoacylglycerol Lipase Prevents Chronic Traumatic Encephalopathy-like Neuropathology in a Mouse Model of Repetitive Mild Closed Head Injury
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Takashima, A. (2008) · Journal of Alzheimer s Disease · doi:10.3233/jad-2008-14403 · Cited by 40
Assessment of Long-Term Effects of Sports-Related Concussions: Biological Mechanisms and Exosomal Biomarkers
Ledreux, A., Pryhoda, M. K., Gorgens, K. A., Shelburne, K. B., Gilmore, A., Linseman, D. A., Fleming, H., Koza, L. A., Campbell, J., Wolff, A., et al. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00761 · Cited by 53
Brain Injury in the Context of Tauopathies
Abisambra, J. F., & Scheff, S. W. (2014) · Journal of Alzheimer s Disease · doi:10.3233/jad-131019 · Cited by 38
“For instance, CCI does not induce tau pathology in wild-type mice, and it only does so in transgenic models where wild type or mutant tau (P301L) is expressed [24, 25, 200].”
Background
Modelling human pathology of traumatic brain injury in animal models
Risling, M., Smith, D. H., Stein, T. D., Thelin, E. P., Zanier, E. R., Ankarcrona, M., & Nilsson, P. (2019) · Journal of Internal Medicine · doi:10.1111/joim.12909 · Cited by 45
An update on the association between traumatic brain injury and Alzheimer’s disease: Focus on Tau pathology and synaptic dysfunction
Li, L., Liang, J., & Fu, H. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.10.020 · Cited by 42
Mechanical Stress as the Common Denominator between Chronic Inflammation, Cancer, and Alzheimer’s Disease
Lévy, M., Moreira, J. D. V., Baronzio, G. F., Dubois, B., Steyaert, J., & Schwartz, L. H. (2015) · Frontiers in Oncology · doi:10.3389/fonc.2015.00197 · Cited by 34
“Reference (79–81) (79–82) (83–91) (92–97) (83, 90, 98, 99) (77, 78, 100) (75–106)”
Repetitive Concussions in Adolescent Athletes – Translating Clinical and Experimental Research into Perspectives on Rehabilitation Strategies
Semple, B. D., Lee, S., Sadjadi, R., Fritz, N. E., Carlson, J., Griep, C., Ho, V., Jang, P., Lamb, A., Popolizio, B., et al. (2015) · Frontiers in Neurology · doi:10.3389/fneur.2015.00069 · Cited by 27
“A commonly used test for cognition in rodents is the Morris water maze (MWM), which specifically evaluates spatial learning and memory [for a detailed description, see Ref.”
BackgroundInfluential
Animal Models of Traumatically-Induced Dementia
Slemmer, J., Hossain, M. Z., & Weber, J. (2011) · Neuromethods · doi:10.1007/978-1-60761-898-0_32 · Cited by 34
Does traumatic brain injury hold the key to the Alzheimer's disease puzzle?
Becker, R. E., Kapogiannis, D., & Greig, N. H. (2017) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2017.11.007 · Cited by 34
“For instance, our TBI model provides accelerated development of neurodegenerative brain pathologies and neuronal compromise and death and can supplement or possibly replace existing models for drug interventions against AD and perhaps other neurodegenerative diseases, as supported by others [33,84,85].”
Background
Mechanical stress models of Alzheimer's disease pathology
Lévy, M., Epelbaum, S., Steyaert, J., Dubois, B., & Schwartz, L. H. (2015) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2015.10.005 · Cited by 37
“Unlike humans with AD, transgenic mouse models based on Ab accumulation do not develop NFTs, yet many do show increased tau hyperphosphorylation [94] (Table 1).”
Influential
Evidence for accelerated tauopathy in the retina of transgenic P301S tau mice exposed to repetitive mild traumatic brain injury
Xu, L., Ryu, J., Nguyen, J. V., Arena, J. D., Rha, E. Y., Vranis, P., Hitt, D., Marsh‐Armstrong, N., & Koliatsos, V. E. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.08.014 · Cited by 35
Progressive Histopathological Damage Occurring Up to One Year after Experimental Traumatic Brain Injury Is Associated with Cognitive Decline and Depression-Like Behavior
Mao, X., Terpolilli, N. A., Wehn, A. C., Cheng, S., Hellal, F., Liu, B., Şeker, F. B., & Plesnila, N. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2019.6510 · Cited by 41
“53 54–69 Recent promising studies already detected important roles for inﬂammatory processes 55,64,65 and cis -phosphorylated tau 62,66–68,70 In order to expand our knowledge about the chronic sequelae of TBI, the current study was therefore not only designed to evaluate histopathological…”
Progressive Cognitive and Post-Traumatic Stress Disorder-Related Behavioral Traits in Rats Exposed to Repetitive Low-Level Blast
Garcia, G. S. P., Perez, G. M., Gasperi, R. D., Sosa, M. A. G., Otero‐Pagan, A., Pryor, D., Abutarboush, R., Kawoos, U., Hof, P. R., Cook, D. G., et al. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2020.7398 · Cited by 37
The Impact of Traumatic Brain Injury on the Aging Brain
Young, J. S., Hobbs, J. G., & Bailes, J. E. (2016) · Current Psychiatry Reports · doi:10.1007/s11920-016-0719-9 · Cited by 36
Traumatic brain injury and the pathways to cerebral tau accumulation
Flavin, W. P., Hosseini, H. C., Ruberti, J. W., Kavehpour, H. P., Giza, C. C., & Prins, M. L. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1239653 · Cited by 33
“RmTBI in a TgT44 mouse model only found 1 animal with neurofibrillary tangles 9 months after injury (125).”
Background
Beneficial association of angiotensin-converting enzyme inhibitors and statins on the occurrence of possible Alzheimer’s disease after traumatic brain injury
Li, M., Reisman, J. I., Morris-Eppolito, B., Qian, S. X., Kazis, L. E., Wolozin, B. L., Goldstein, L. E., & Xia, W. (2020) · Alzheimer s Research & Therapy · doi:10.1186/s13195-020-00589-3 · Cited by 65
A model of recurrent concussion that leads to long-term motor deficits, CTE-like tauopathy and exacerbation of an ALS phenotype
Thomsen, G. M., Ma, A. M., Ko, A., Harada, M. Y., Wyss, L., Haro, P. S., Vit, J.-P., Shelest, O., Rhee, P., Svendsen, C. N., et al. (2016) · Journal of Trauma and Acute Care Surgery · doi:10.1097/ta.0000000000001248 · Cited by 28
“Injury intervals were designed to allow for recovery from the acute symptoms of mild TBI between injury events and are similar to previously reported repetitive injury models.(13)”
BackgroundResult
Neuronal BAG3 attenuates tau hyperphosphorylation, synaptic dysfunction, and cognitive deficits induced by traumatic brain injury via the regulation of autophagy-lysosome pathway
Sweeney, N., Kim, T. Y., Morrison, C. T., Li, L., Acosta, D. M., Liang, J., Datla, N. V., Fitzgerald, J. A., Huang, H., Liu, X., et al. (2024) · Acta Neuropathologica · doi:10.1007/s00401-024-02810-1 · Cited by 28
“Previous reports indicate that TBI increases tau pathology in several mouse models [23, 27, 44, 45, 66, 74, 91, 97, 107, 112].”
Background
Repetitive Concussive and Subconcussive Injury in a Human Tau Mouse Model Results in Chronic Cognitive Dysfunction and Disruption of White Matter Tracts, But Not Tau Pathology
Gangolli, M., Benetatos, J., Esparza, T. J., Fountain, E. M., Seneviratne, S., & Brody, D. L. (2018) · Journal of Neurotrauma · doi:10.1089/neu.2018.5700 · Cited by 28
“12 More recent work found that while repetitive closed headed impacts caused progressive behavioral impairments and neuroinﬂammation, there was no ptau pathology at chronic time-points up to 6 and 12 months post-injury using immunohistochemistry methods.”
Drug Abuse, Brain Calcification and Glutamate-Induced Neurodegeneration
Rodríguez, M. J., Pugliese, M., & Mahy, N. (2009) · Current Drug Abuse Reviews · doi:10.2174/1874473710902010099 · Cited by 26
“Acute neurological injury and chronic brain damage has been related in boxing participants, with a correlation in the prevalence of subdural hematoma and dementia pugilistica [127;128].”
Background
Mechanical stress increases brain amyloid β, tau, and α‐synuclein concentrations in wild‐type mice
Lévy, M., Hamraz, M., Abolhassani, M., Bigan, E., Lafitte, O. D., Steyaert, J., Dubois, B., & Schwartz, L. H. (2017) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2017.11.003 · Cited by 29
“Unlike our results, one study using wild-type mice subjected to rmTBI (4!/day, 1 day/week for 4 weeks) did not reproduce postinjury tau changes [11].”
BackgroundResult
Modeling Chronic Traumatic Encephalopathy: The Way Forward for Future Discovery
Turner, R. C., Lucke-Wold, B. P., Logsdon, A. F., Robson, M. J., Lee, J. M., Bailes, J. E., Dashnaw, M. L., Huber, J. D., Petraglia, A. L., & Rosen, C. L. (2015) · Frontiers in Neurology · doi:10.3389/fneur.2015.00223 · Cited by 25
“The affected mouse displayed neuropathological changes that included heightened tau burden, the presence of NFTs, and cognitive deficits (35).”
BackgroundInfluential
Chronic Traumatic Encephalopathy: A Critical Appraisal
Levin, B., & Bhardwaj, A. (2013) · Neurocritical Care · doi:10.1007/s12028-013-9931-1 · Cited by 22
“The mouse that developed cognitive impairment had increased iron deposits in the ventral cortical regions which may have increased NFT deposition leading to the speculation that perivascular hemorrhages found in boxers may lead to a similar process [20].”
Background
A High-Throughput Screening Assay for Determining Cellular Levels of Total Tau Protein
Dehdashti, S., Zheng, W., Gever, J. R., Wilhelm, R. S., Nguyễn, Ð.-T., Sittampalam, G. S., McKew, J. C., Austin, C. P., & Prusiner, S. B. (2013) · Current Alzheimer Research · doi:10.2174/15672050113109990143 · Cited by 23
“frontotemporal dementias (FTDs), traumatic brain injury (TBI), chronic traumatic encephalopathy (CTE), progressive supranuclear palsy (PSP) and Niemann-Pick type C (NPC) (1, 2).”
Background
Tau Pathology, Metal Dyshomeostasis and Repetitive Mild Traumatic Brain Injury: An Unexplored Link Paving the Way for Neurodegeneration
Juan, S. M. A., Daglas, M., & Adlard, P. A. (2022) · Journal of Neurotrauma · doi:10.1089/neu.2021.0241 · Cited by 21
Cytoskeletal protein α–II spectrin degradation in the brain of repeated blast exposed mice
Valiyaveettil, M., Alamneh, Y. A., Wang, Y., Arun, P., Oguntayo, S., Wei, Y., Long, J. B., & Nambiar, M. P. (2014) · Brain Research · doi:10.1016/j.brainres.2013.12.031 · Cited by 25
Traumatic Brain Injury-related voiding dysfunction in mice is caused by damage to rostral pathways, altering inputs to the reflex pathways
Albayram, Ö., MacIver, B., Mathai, J., Verstegen, A. M. J., Baxley, S., Qiu, C., Bell, C. A., Caldarone, B. J., Zhou, X. Z., Lu, K. P., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-45234-8 · Cited by 26
The hidden variables problem in Alzheimer's disease clinical trial design
Liyanage, S., Santos, C., & Weaver, D. F. (2018) · Alzheimer's & Dementia · doi:10.1016/j.trci.2018.09.003 · Cited by 20
“In Tg2576 murine models, repeated brain injuries were directly associated with a significant increase in neurofibrillary tangles, cerebral atrophy, and cognitive deficits [21].”
Background
Mild repetitive head impacts alter perivascular flow in the midbrain dopaminergic system in awake rats
Cai, X., Harding, I. C., Sadaka, A. H., Colarusso, B. A., Kulkarni, P., Ebong, E. E., Qiao, J., O'Hare, N. R., & Ferris, C. F. (2021) · Brain Communications · doi:10.1093/braincomms/fcab265 · Cited by 22
Chlorzoxazone exhibits neuroprotection against Alzheimer’s disease by attenuating neuroinflammation and neurodegeneration in vitro and in vivo
Bai, Y., & Ma, X. (2020) · International Immunopharmacology · doi:10.1016/j.intimp.2020.106790 · Cited by 21
Naloxone exacerbates memory impairments and depressive-like behavior after mild traumatic brain injury (mTBI) in mice with upregulated opioid system activity
Leśniak, A., Leszczyński, P., Bujalska‐Zadrożny, M., Pick, C. G., & Sacharczuk, M. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.03.015 · Cited by 20
The utility of clinical criteria in patients with chronic traumatic encephalopathy
Laffey, M., Darby, A. J., Cline, M. G., Teng, E., & Mendez, M. F. (2018) · Neurorehabilitation · doi:10.3233/nre-182452 · Cited by 18
“…Stewart, & Smith, 2012; Lakis, Corona, Toshkezi, & Chin, 2013; McCrory, Meeuwisse, Kutcher, Jordan, & Gardner, 2013; McKee et al., 2009; McKee et al., 2013; Schmidt, Zhukareva, Newell, Lee, & Trojanowski, 2001; Smith, Johnson, & Stewart, 2013; Sponheim et al., 2011; Yoshiyama et al., 2005).”
Tau overexpression exacerbates neuropathology after repeated mild head impacts in male mice
Cheng, H., Deaton, L. M., Qiu, M., Ha, S., Pacoma, R., Lao, J., Tolley, V., Moran, R., Keeton, A., Lamb, J. R., et al. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104683 · Cited by 16
“In the literature, there is inconsistency for rmTBI to induce tauopathy in rodents, especially in a C57BL/6 background [62-66].”
Literature-Related Discovery (LRD)
Kostoff, R. N., Block, J. A., Solka, J. L., Briggs, M. B., Rushenberg, R. L., Stump, J. A., Johnson, D., Lyons, T. J., & Wyatt, J. R. (2007) · Defense Technical Information Center (DTIC) · doi:10.21236/ada473438 · Cited by 19
Prion-Like Propagation Mechanisms in Tauopathies and Traumatic Brain Injury: Challenges and Prospects
Alyenbaawi, H., Allison, W. T., & Mok, S. (2020) · Biomolecules · doi:10.3390/biom10111487 · Cited by 20
Quantitative Imaging of Blood-Brain Barrier Permeability Following Repetitive Mild Head Impacts
Leaston, J., Qiao, J., Harding, I. C., Kulkarni, P., Gharagouzloo, C. A., Ebong, E. E., & Ferris, C. F. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.729464 · Cited by 18
Repetitive Traumatic Brain Injury Causes Neuroinflammation before Tau Pathology in Adolescent P301S Mice
Izzy, S., Brown-Whalen, A., Yahya, T., Sarro-Schwartz, A., Jin, G., Chung, J. Y., Lüle, S., Morsett, L. M., Alquraini, A., Wu, L., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22020907 · Cited by 16
“Unlike contusion TBI, the formation of tau misfolded aggregates may take a longer time to develop after rCHI which exhibits a distinct immune response from the one that accompanies CCI and cerebral contusion [24,52].”
Background
Pattern of Injury with a Graded Excitotoxic Insult and Ensuing Chronic Medial Septal Damage in the Rat Brain
Rodríguez, M. J., Prats, A., Malpesa, Y., Andrés, N., Pugliese, M., Batlle, M., & Mahy, N. (2009) · Journal of Neurotrauma · doi:10.1089/neu.2008.0553 · Cited by 13
“Previous studies done with quisqualic or ibotenic acid under similar conditions, found a similarly severe atrophy of the medial septum after a 1-year period (Ramani et al., 2006; Yoshiyama et al., 2005; Leutgeb and Mizumori, 1999; Mahy et al., 1995).”
Therapeutic Approaches for the Treatment of Alzheimer's Disease: An Overview
Lau, L., & Brodney, M. A. (2007) · Springer eBooks · doi:10.1007/7355_2007_017 · Cited by 8
Traumatic Brain Injury and Chronic Traumatic Encephalopathy: Not Only Trigger for Neurodegeneration but Also for Cerebral Amyloid Angiopathy?
Zedde, M., Piazza, F., & Pascarella, R. (2025) · Biomedicines · doi:10.3390/biomedicines13040881 · Cited by 12
“Only one mouse exhibited accelerated tau deposition [80].”
Impact of nutrition on inflammation, tauopathy, and behavioral outcomes from chronic traumatic encephalopathy
Yu, J., Zhu, H., Taheri, S., Mondy, W. L., Perry, S. J., & Kindy, M. S. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1312-4 · Cited by 18
“The microglial activation and reactive astrocytosis are probably the result of the primary injury, the repetitive mTBI, and the consequences of a progressive, chronic neuroinflammatory condition that contributes to secondary and potentially tertiary responses [44].”
Catastrophic consequences: can the feline parasite Toxoplasma gondii prompt the purrfect neuroinflammatory storm following traumatic brain injury?
Baker, T. L., Sun, M., Semple, B. D., Tyebji, S., Tonkin, C. J., Mychasiuk, R., & Shultz, S. R. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01885-3 · Cited by 11
Repeat Closed-Head Injury in Male Rats Impairs Attention but Causes Heterogeneous Outcomes in Multiple Measures of Impulsivity and Glial Pathology
Haar, C. V., Wampler, S. K., Bhatia, H., Ozga, J. E., Toegel, C., Lake, A. D., Iames, C. W., Cabral, C., & Martens, K. M. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.809249 · Cited by 9
Molecular intersections of traumatic brain injury and Alzheimer’s disease: the role of ADMSC-derived exosomes and hub genes in microglial polarization
Li, P., Ye, L., Sun, S., Wang, Y., Chen, Y., Chang, J., Yin, R., Liu, X., Zuo, W., Xu, H., et al. (2024) · Metabolic Brain Disease · doi:10.1007/s11011-024-01503-8 · Cited by 7

Authors: Yoshiyama, Y., Uryu, K., Higuchi, M., Longhi, L., Hoover, R., Fujimoto, S., McIntosh, T., Lee, V. M.-Y., & Trojanowski, J. Q.
Affiliations: University of Pennsylvania (US)
Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico (IT)
ORCID: Yoshiyama, Yasumasa
Uryu, Kunihiro
Higuchi, Makoto
McIntosh, Tracy
Lee, Virginia M.-Y.
Trojanowski, John Q.
Venue: Journal of Neurotrauma
Publisher: SAGE Publications
Published: 2005-10
Volume: 22
Issue: 10
Pages: 1134-1141
ISSN: 0897-7151 (ISSN-L)
1557-9042
DOI: 10.1089/neu.2005.22.1134
OpenAlex: W2059869018
Cited by: 133
References: 0
Citations by year: 2026: 1 · 2025: 2 · 2024: 3 · 2023: 4 · 2022: 4 · 2021: 4 · 2020: 9 · 2019: 12 · 2018: 10 · 2017: 8 · 2016: 10 · 2015: 13 · 2014: 11 · 2013: 14 · 2012: 4
FWCI: 2.00
Type: journal article
Language: en
Open access: closed
Licence: www.liebertpub.com/nv/resources-tools/text-and-data-mining-policy/121/ (tdm)
Locations: Journal of Neurotrauma (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Neurological Disorders and Stroke (P50NS008803, NS P50-08803, NS R01-40978)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury Research
Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury and Neurovascular Disturbances
Keywords: repetitive mild traumatic brain injury, chronic traumatic encephalopathy, neurofibrillary tangles, tau pathology, brain atrophy, cognitive impairment, concussion, Alzheimer's disease, transgenic mouse model, amyloid-beta, amyloid plaques
MeSH terms: Animals, Atrophy, Brain Injuries, Cerebral Cortex, Cognition Disorders, Disease Models, Animal, Humans, Immunohistochemistry, Mice, Transgenic, Blotting, Western, Neurofibrillary Tangles, tau Proteins, Maze Learning, Tauopathies, Mice

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Enhanced Neurofibrillary Tangle Formation, Cerebral Atrophy, and Cognitive Deficits Induced by Repetitive Mild Brain Injury in a Transgenic Tauopathy Mouse Model

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