A novel, ultrasensitive assay for tau: potential for assessing traumatic brain injury in tissues and biofluids.

Rubenstein, Richard; Chang, Binggong; Davies, Peter; Wagner, Amy K.; Robertson, Claudia S.; Wang, Kevin K.W.

doi:10.1089/neu.2014.3548

Cited by 116Traumatic Brain Injury ResearchTraumatic Brain Injury and Neurovascular DisturbancesAlzheimer's disease research and treatments

A novel, ultrasensitive assay for tau: potential for assessing traumatic brain injury in tissues and biofluids.

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Rubenstein, Richard, Chang, Binggong, Davies, Peter, Wagner, Amy K., Robertson, Claudia S., Wang, Kevin K.W.·2015·Journal of Neurotrauma

DOI 10.1089/neu.2014.3548PMC PMC4348038

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Abstract

Traumatic brain injury (TBI) is a cause of death and disability and can lead to tauopathy-related dementia at an early age. Pathologically, TBI results in axonal injury that is coupled to tau hyperphosphorylation, leading to microtubule instability and tau-mediated neurodegeneration. This suggests that the forms of this protein might serve as neuroinjury-related biomarkers for diagnosis of injury severity and prognosis of the neurological damage prior to clinical expression. We initially determined whether we could detect tau in body fluids using a highly sensitive assay. We used a novel immunoassay, enhanced immunoassay using multi-arrayed fiberoptics (EIMAF) either alone or in combination with rolling circle amplification (a-EIMAF) for the detection of total (T) and phosphorylated (P) tau proteins from brains and biofluids (blood, CSF) of rodents following controlled cortical impact (CCI) and human patients post severe TBI (sTBI). This assay technology for tau is the most sensitive to date with a detection limit of approximately 100 ag/mL for either T-tau and P-tau. In the rodent models, T-tau and P-tau levels in brain and blood increased following CCI during the acute phase and remained high during the chronic phase (30 d). In human CSF samples, T-tau and P-tau increased during the sampling period (5-6 d). T-tau and P-tau in human serum rose during the acute phase and decreased during the chronic stage but was still detectable beyond six months post sTBI. Thus, EIMAF has the potential for assessing both the severity of the proximal injury and the prognosis using easily accessible samples.

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Tau hyperphosphorylation is consistently present in the initial and long-term secondary mechanisms initiated by traumatic brain injury.
“Tau hyperphosphorylation is also consistently present in the initial and long-term secondary mechanisms initiated by traumatic brain injury (TBI) (Petraglia et al., 2014; Zheng et al., 2014; Rubenstein et al., 2015; Ali et al., 2019; Tan et al., 2020), a leading cause of morbidity and mortality worldwide (Hay et al., 2016).”
From Tauopathy and Epilepsy Comorbidities and Underlying Mechanisms (2022) · cites this paper as Rubenstein et al., 2015
The Results report elevated phosphorylated tau in the acute phase after severe TBI and in most serum samples collected up to approximately six months later. However, the Discussion says its relationship to the acute injury cascade remains unclear. The paper supports an acute and longer-term association, not consistent presence throughout TBI’s secondary mechanisms. (LLM, conf=0.86)
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Neuron-Specific Enolase Serum Levels After Controlled Cortical Impact Injury in the Rat
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Traumatic brain injury: integrated approaches to improve prevention, clinical care, and research
Maas, A. I. R., Menon, D. K., Adelson, P. D., Andelic, N., Bell, M. J., Belli, A., Bragge, P., Brazinova, A., Büki, A., Chesnut, R. M., et al. (2017) · The Lancet Neurology · doi:10.1016/s1474-4422(17)30371-x · Cited by 2,609 · see citing works
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Traumatic brain injuries
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Blood phospho-tau in Alzheimer disease: analysis, interpretation, and clinical utility
Karikari, T. K., Ashton, N. J., Brinkmalm, G., Brum, W. S., Benedet, A. L., Montoliu‐Gaya, L., Lantero‐Rodriguez, J., Pascoal, T. A., Suárez‐Calvet, M., Rosa‐Neto, P., et al. (2022) · Nature Reviews Neurology · doi:10.1038/s41582-022-00665-2 · Cited by 327 · see citing works
Comparing Plasma Phospho Tau, Total Tau, and Phospho Tau–Total Tau Ratio as Acute and Chronic Traumatic Brain Injury Biomarkers
Rubenstein, R., Chang, B., Yue, J. K., Chiu, A., Winkler, E. A., Puccio, A. M., Diaz-Arrastia, R. R., Yuh, E. L., Mukherjee, P., Valadka, A. B., et al. (2017) · JAMA Neurology · doi:10.1001/jamaneurol.2017.0655 · Cited by 262 · see citing works
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Peripheral Total Tau in Military Personnel Who Sustain Traumatic Brain Injuries During Deployment
Olivera, A., Lejbman, N., Jeromin, A., French, L. M., Kim, H., Cashion, A. K., Mysliwiec, V., Diaz-Arrastia, R. R., & Gill, J. (2015) · JAMA Neurology · doi:10.1001/jamaneurol.2015.1383 · Cited by 157 · see citing works
Tau Pathology in Chronic Traumatic Encephalopathy and Alzheimer's Disease: Similarities and Differences
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Blood biomarkers for mild traumatic brain injury: a selective review of unresolved issues
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Current status of fluid biomarkers in mild traumatic brain injury
Kulbe, J. R., & Geddes, J. W. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.05.004 · Cited by 124 · see citing works
Assessing Neuronal and Astrocyte Derived Exosomes From Individuals With Mild Traumatic Brain Injury for Markers of Neurodegeneration and Cytotoxic Activity
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Biomarkers of Traumatic Brain Injury: Temporal Changes in Body Fluids
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Blood biomarkers for traumatic brain injury: A narrative review of current evidence
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Role of Caspase-3-Mediated Apoptosis in Chronic Caspase-3-Cleaved Tau Accumulation and Blood–Brain Barrier Damage in the Corpus Callosum after Traumatic Brain Injury in Rats
Glushakova, O. Y., Glushakov, A. O., Borlongan, C. V., Valadka, A. B., Hayes, R. L., & Glushakov, A. V. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2017.4999 · Cited by 91 · see citing works
Traumatic brain injury triggers APP and Tau cleavage by delta-secretase, mediating Alzheimer’s disease pathology
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The game changer: UCH-L1 and GFAP-based blood test as the first marketed in vitro diagnostic test for mild traumatic brain injury
Kobeissy, F. H., Arja, R. D., Munoz, J. C., Shear, D. A., Gilsdorf, J. S., Zhu, J., Yadikar, H., Haskins, W. E., Tyndall, J., & Wang, K. (2024) · Expert Review of Molecular Diagnostics · doi:10.1080/14737159.2024.2306876 · Cited by 72 · see citing works
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Temporal MRI characterization, neurobiochemical and neurobehavioral changes in a mouse repetitive concussive head injury model
Yang, Z., Wang, P., Morgan, D., Bruijnzeel, A. W., Lin, D., Pan, J., Lin, F. Y., Strang, K. H., Selig, T. M., Pérez, P. D., et al. (2015) · Scientific Reports · doi:10.1038/srep11178 · Cited by 68 · see citing works
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Significance of Blood and Cerebrospinal Fluid Biomarkers for Alzheimer’s Disease: Sensitivity, Specificity and Potential for Clinical Use
d’Abramo, C., D'adamio, L., & Giliberto, L. (2020) · Journal of Personalized Medicine · doi:10.3390/jpm10030116 · Cited by 68 · see citing works
Lithium as a Treatment for Alzheimer’s Disease: The Systems Pharmacology Perspective
Hampel, H. J., Lista, S., Mango, D., Nisticò, R., Perry, G. L., Ávila, J., Hernández, F., Geerts, H., Vergallo, A., (APMI), A. P. M. I., et al. (2019) · Journal of Alzheimer s Disease · doi:10.3233/jad-190197 · Cited by 65 · see citing works
Ultrasensitive assays for detection of plasma tau and phosphorylated tau 181 in Alzheimer’s disease: a systematic review and meta-analysis
Ding, X., Zhang, S., Jiang, L., Wang, L., Li, T., & Lei, P. (2021) · Translational Neurodegeneration · doi:10.1186/s40035-021-00234-5 · Cited by 60 · see citing works
Neurofilament light chain and total tau in the differential diagnosis and prognostic evaluation of acute and chronic inflammatory polyneuropathies
Kmezic, I., Samuelsson, K., Finn, A., Upate, Z., Blennow, K., Zetterberg, H., & Press, R. (2022) · European Journal of Neurology · doi:10.1111/ene.15428 · Cited by 54 · see citing works
KCNJ2 inhibition mitigates mechanical injury in a human brain organoid model of traumatic brain injury
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Functional and Molecular Correlates after Single and Repeated Rat Closed-Head Concussion: Indices of Vulnerability after Brain Injury
Mountney, A., Boutté, A. M., Cartagena, C. M., Flerlage, W. J., Johnson, W. D., Rho, C., Lu, X.-C., Yarnell, A. M., Marcsisin, S. R., Sousa, J. C., et al. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2016.4679 · Cited by 49 · see citing works
Operation Brain Trauma Therapy: 2016 Update
Kochanek, P. M., Bramlett, H. M., Dixon, C. E., Dietrich, W. D., Mondello, S., Wang, K., Hayes, R. L., Lafrenaye, A. D., Povlishock, J. T., Tortella, F. C., et al. (2018) · Military Medicine · doi:10.1093/milmed/usx184 · Cited by 44 · see citing works
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Blood-based traumatic brain injury biomarkers – Clinical utilities and regulatory pathways in the United States, Europe and Canada
Wang, K., Pareja, J. C. M., Mondello, S., Diaz-Arrastia, R. R., Wellington, C. L., Kenney, K., Puccio, A. M., Hutchison, J. S., McKinnon, N. K., Okonkwo, D. O., et al. (2021) · Expert Review of Molecular Diagnostics · doi:10.1080/14737159.2021.2005583 · Cited by 47 · see citing works
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“Sigma-1 receptor modulation by clemastine highlights its repurposing as neuroprotective agent against seizures and cognitive deficits in PTZ-kindled rats”
Badawi, G. A., Shokr, M. M., Elshazly, S. M., Zaki, H. F., & Mohamed, A. F. (2024) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2024.176851 · Cited by 39 · see citing works
Novel Mouse Tauopathy Model for Repetitive Mild Traumatic Brain Injury: Evaluation of Long-Term Effects on Cognition and Biomarker Levels After Therapeutic Inhibition of Tau Phosphorylation
Rubenstein, R., Sharma, D. R., Chang, B., Oumata, N., Cam, M., Vaucelle, L., Lindberg, M. F., Chiu, A., Wısnıewskı, T., Wang, K., et al. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00124 · Cited by 38 · see citing works
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Copenhagen Head Injury Ciclosporin Study: A Phase IIa Safety, Pharmacokinetics, and Biomarker Study of Ciclosporin in Severe Traumatic Brain Injury Patients
Kelsen, J., Karlsson, M., Hansson, M. J., Yang, Z., Fischer, W., Hugerth, M., Nordström, C., Åstrand, R., Keep, M. F., Kilbaugh, T. J., et al. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.6369 · Cited by 37 · see citing works
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Current Opportunities for Clinical Monitoring of Axonal Pathology in Traumatic Brain Injury
Tsitsopoulos, P. P., Hamdeh, S. A., & Marklund, N. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00599 · Cited by 37 · see citing works
Association between single moderate to severe traumatic brain injury and long-term tauopathy in humans and preclinical animal models: a systematic narrative review of the literature
Walker, A. P., Chapin, B. A., Abisambra, J. F., & DeKosky, S. T. (2022) · Acta Neuropathologica Communications · doi:10.1186/s40478-022-01311-0 · Cited by 36 · see citing works
Tauopathy and Epilepsy Comorbidities and Underlying Mechanisms
Hwang, K., Vaknalli, R. N., Addo-Osafo, K., Vicente, M., & Vossel, K. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.903973 · Cited by 35 · see citing works
Exploiting blood-based biomarkers to align preclinical models with human traumatic brain injury
Lisi, I., Moro, F., Mazzone, E., Marklund, N., Pischiutta, F., Kobeissy, F. H., Mao, X., Corrigan, F., Helmy, A. E., Nasrallah, F. A., et al. (2024) · Brain · doi:10.1093/brain/awae350 · Cited by 33 · see citing works
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Concentration of microtubule associated protein tau (MAPT) in urine and saliva as a potential biomarker of traumatic brain injury in relationship with blood–brain barrier disruption in postmortem examination
Olczak, M., Poniatowski, Ł. A., Niderla‐Bielińska, J., Kwiatkowska, M., Chutorański, D., Tarka, S., & Wierzba‐Bobrowicz, T. (2019) · Forensic Science International · doi:10.1016/j.forsciint.2019.05.010 · Cited by 32 · see citing works
Omega-3 Fatty Acids and Vitamin D Decrease Plasma T-Tau, GFAP, and UCH-L1 in Experimental Traumatic Brain Injury
Scrimgeour, A. G., Condlin, M. L., Loban, A., & DeMar, J. C. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.685220 · Cited by 32 · see citing works
Profiling biomarkers of traumatic axonal injury: From mouse to man
Manivannan, S., Makwana, M., Ahmed, A. I., & Zaben, M. (2018) · Clinical Neurology and Neurosurgery · doi:10.1016/j.clineuro.2018.05.017 · Cited by 30 · see citing works
Overpressure Exposure From .50-Caliber Rifle Training Is Associated With Increased Amyloid Beta Peptides in Serum
Thangavelu, B., LaValle, C. R., Egnoto, M. J., Nemes, J., Boutté, A. M., & Kamimori, G. H. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00620 · Cited by 30 · see citing works
Hyperphosphorylated Tau as a Novel Biomarker for Traumatic Axonal Injury in the Spinal Cord
Caprelli, M. T., Mothe, A. J., & Tator, C. H. (2018) · Journal of Neurotrauma · doi:10.1089/neu.2017.5495 · Cited by 29 · see citing works
Serum assessment of traumatic axonal injury: the correlation of GFAP, t-Tau, UCH-L1, and NfL levels with diffusion tensor imaging metrics and its prognosis utility
Castaño-León, A. M., Carabias, C. S., Hilario, A., Ramos, A., Navarro-Main, B., Paredes, I., Munarriz, P. M., Panero, I., Fernández, C. E., García‐Pérez, D., et al. (2022) · Journal of neurosurgery · doi:10.3171/2022.5.jns22638 · Cited by 29 · see citing works
Neuroproteomics and Systems Biology Approach to Identify Temporal Biomarker Changes Post Experimental Traumatic Brain Injury in Rats
Kobeissy, F. H., Guingab-Cagmat, J. D., Zhang, Z., Moghieb, A. M., Glushakova, O. Y., Mondello, S., Boutté, A. M., Anagli, J. Y., Rubenstein, R., Bahmad, H. F., et al. (2016) · Frontiers in Neurology · doi:10.3389/fneur.2016.00198 · Cited by 29 · see citing works
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Temporal Profiles of P-Tau, T-Tau, and P-Tau:Tau Ratios in Cerebrospinal Fluid and Blood from Moderate-Severe Traumatic Brain Injury Patients and Relationship to 6–12 Month Global Outcomes
Rubenstein, R., McQuillan, L. E., Wang, K., Robertson, C. S., Chang, B., Yang, Z., Xu, H., Williamson, J. B., & Wagner, A. K. (2023) · Journal of Neurotrauma · doi:10.1089/neu.2022.0479 · Cited by 28 · see citing works
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Proposed mechanisms of tau: relationships to traumatic brain injury, Alzheimer’s disease, and epilepsy
Martin, S. P., & Leeman-Markowski, B. A. (2024) · Frontiers in Neurology · doi:10.3389/fneur.2023.1287545 · Cited by 28 · see citing works
Serum τ protein as a potential biomarker in the assessment of traumatic brain injury
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Neuroprognostication after cardiac arrest in the light of targeted temperature management
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An investigation of neuroinjury biomarkers after sport-related concussion: from the subacute phase to clinical recovery
Battista, A. P. D., Rhind, S. G., BAKER, A. J., Jetly, R., Debad, J. D., Richards, D. W., & Hutchison, M. G. (2018) · Brain Injury · doi:10.1080/02699052.2018.1432892 · Cited by 27 · see citing works
Developing Biomarkers of Mild Traumatic Brain Injury: Promise and Progress of CNS-Derived Exosomes
Vaughn, M. N., Winston, C. N., Levin, N., Rissman, R. A., & Risbrough, V. B. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2021.698206 · Cited by 26 · see citing works
TBI Rehabilomics Research: Conceptualizing a humoral triad for designing effective rehabilitation interventions
Wagner, A. K., & Kumar, R. G. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.09.011 · Cited by 25 · see citing works
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Penetrating Traumatic Brain Injury Triggers Dysregulation of Cathepsin B Protein Levels Independent of Cysteine Protease Activity in Brain and Cerebral Spinal Fluid
Boutté, A. M., HOOK, V. Y. H., Thangavelu, B., Sarkis, G. A., Abbatiello, B. N., Hook, G., Jacobsen, J. S., Robertson, C. S., Gilsdorf, J. S., Yang, Z., et al. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2019.6537 · Cited by 25 · see citing works
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A systematic review of large animal models of combined traumatic brain injury and hemorrhagic shock
Mayer, A. R., Dodd, A. B., Vermillion, M. S., Stephenson, D. D., Chaudry, I. H., Bragin, D. E., Gigliotti, A. P., Dodd, R. J., Wasserott, B. C., Shukla, P., et al. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.06.024 · Cited by 23 · see citing works
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 23 · see citing works
Elevated cerebrospinal fluid total tau in former professional athletes with multiple concussions
Taghdiri, F., Multani, N., Tarazi, A., Naeimi, S. A., Khodadadi, M., Esopenko, C., Green, R., Colella, B., Wennberg, R. A., Mikulis, D. J., et al. (2019) · Neurology · doi:10.1212/wnl.0000000000007608 · Cited by 23 · see citing works
Protein profile changes in the frontotemporal lobes in human severe traumatic brain injury
Xu, B., Tian, R., Wang, X., Zhan, S., Wang, R., Guo, Y., & Ge, W. (2016) · Brain Research · doi:10.1016/j.brainres.2016.04.008 · Cited by 22 · see citing works
The diagnostic potential of fluid and imaging biomarkers in chronic traumatic encephalopathy (CTE)
Bergauer, A., van Osch, R., van Elferen, S., Gyllvik, S., Venkatesh, H., & Schreiber, R. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.112602 · Cited by 22 · see citing works
Suppression of BACE1 and amyloidogenic/RAGE axis by sitagliptin ameliorates PTZ kindling-induced cognitive deficits in rats
Safar, M. M., Shahin, N. N., Mohamed, A. F., & Abdelkader, N. F. (2020) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2020.109144 · Cited by 20 · see citing works
Research Frontiers in Traumatic Brain Injury
Gardner, A. J., Shih, S. L., Adamov, E. V., & ZAFONTE, R. D. (2017) · Physical Medicine and Rehabilitation Clinics of North America · doi:10.1016/j.pmr.2016.12.014 · Cited by 19 · see citing works
An Introduction to Ultrasensitive Assays for Plasma Tau Detection
Ding, X., Tuo, Q., & Lei, P. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-201499 · Cited by 19 · see citing works
Plasma phosphorylated tau181 as a biomarker of mild traumatic brain injury: findings from THINC and NCAA-DoD CARE Consortium prospective cohorts
Devoto, C., Vorn, R., Mithani, S., Meier, T. B., Lai, C., Broglio, S. P., McAllister, T. W., Giza, C. C., Huber, D. L., Harezlak, J., et al. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1202967 · Cited by 17 · see citing works
Tau: a biomarker of Huntington’s disease
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Prion-Like Propagation Mechanisms in Tauopathies and Traumatic Brain Injury: Challenges and Prospects
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Quantification of Tau-A in serum after brain injury: a comparison of two analytical platforms, ELISA and electrochemiluminescence immunoassay
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Authors: Rubenstein, R., Chang, B., Davies, P., Wagner, A. K., Robertson, C. S., & Wang, K. K. W.
Affiliations: SUNY Downstate Health Sciences University (US)
Feinstein Institute for Medical Research (US)
University of Pittsburgh Medical Center (US)
Baylor College of Medicine (US)
University of Florida (US)
Corresponding author: Rubenstein, Richard
ORCID: Rubenstein, Richard
Davies, Peter
Wagner, Amy K.
Robertson, Claudia S.
Wang, Kevin K.W.
Venue: Journal of Neurotrauma
Publisher: SAGE Publications
Published: 2015-03
Volume: 32
Issue: 5
Pages: 342-352
ISSN: 0897-7151 (ISSN-L)
1557-9042
DOI: 10.1089/neu.2014.3548
PMC: PMC4348038
OpenAlex: W2006643577
Cited by: 116
References: 90
Citations by year: 2026: 2 · 2025: 5 · 2024: 9 · 2023: 14 · 2022: 16 · 2021: 15 · 2020: 11 · 2019: 11 · 2018: 8 · 2017: 12 · 2016: 7 · 2015: 5 · 2014: 1
FWCI: 6.31
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.liebertpub.com/nv/resources-tools/text-and-data-mining-policy/121/ (tdm)
Locations: Journal of Neurotrauma (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Keywords: tau protein, tau phosphorylation, traumatic brain injury, biomarkers, rolling circle amplification, cerebrospinal fluid, serum, controlled cortical impact, axonal injury, tauopathy, neurodegeneration, injury severity assessment, prognosis
MeSH terms: Animals, Brain Injuries, Humans, Immunoassay, Mice, Inbred C57BL, Sensitivity and Specificity, Immunoblotting, Biomarkers, tau Proteins, Rats, Sprague-Dawley, Mice, Rats

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A novel, ultrasensitive assay for tau: potential for assessing traumatic brain injury in tissues and biofluids.

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