Neuroprotection for traumatic brain injury: translational challenges and emerging therapeutic strategies

Loane, David J.; Faden, Alan I.

doi:10.1016/j.tips.2010.09.005

Cited by 574Traumatic Brain Injury and Neurovascular DisturbancesTraumatic Brain Injury ResearchAutomotive and Human Injury Biomechanics

Neuroprotection for traumatic brain injury: translational challenges and emerging therapeutic strategies

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Loane, David J., Faden, Alan I.·2010·Trends in Pharmacological Sciences

DOI 10.1016/j.tips.2010.09.005PMC PMC2999630

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Abstract

Traumatic brain injury (TBI) causes secondary biochemical changes that contribute to subsequent tissue damage and associated neuronal cell death. Neuroprotective treatments that limit secondary tissue loss and/or improve behavioral outcome have been well established in multiple animal models of TBI. However, translation of such neuroprotective strategies to human injury have been disappointing, with the failure of more than thirty controlled clinical trials. Both conceptual issues and methodological differences between preclinical and clinical injury have undoubtedly contributed to these translational difficulties. More recently, changes in experimental approach, as well as altered clinical trial methodologies, have raised cautious optimism regarding the outcomes of future clinical trials. Here we critically review developing experimental neuroprotective strategies that show promise, and we propose criteria for improving the probability of successful clinical translation.

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The failure of pre-clinical TBI therapies to translate has been attributed in part to inadequate preclinical efforts to recapitulate the complexity of the human injury.
“This has been attributed in part to inadequate preclinical efforts to recapitulate the complexity of the human injury.”
From Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know (2019) · cites this paper as [18]

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Chen, S.-F., Hung, T., Chen, C.-C., Lin, K.-H., Huang, Y.-N., Tsai, H.-C., & Wang, J. (2007) · Life Sciences · doi:10.1016/j.lfs.2007.05.023 · Cited by 118 · see citing works
Multiple Caspases Are Activated after Traumatic Brain Injury: Evidence for Involvement in Functional Outcome
Knoblach, S. M., Nikolaeva, M. A., Huang, X., Fan, L., Krajewski, S., Reed, J. C., & Faden, A. I. (2002) · Journal of Neurotrauma · doi:10.1089/08977150260337967 · Cited by 117 · see citing works
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Comparative Neuroprotective Effects of Cyclosporin a and NIM811, a Nonimmunosuppressive Cyclosporin a Analog, following Traumatic Brain Injury
Mbye, L. H., Singh, I. N., Carrico, K. M., Saatman, K. E., & Hall, E. D. (2008) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2008.93 · Cited by 115 · see citing works
Progesterone Differentially Regulates Pro- and Anti-Apoptotic Gene Expression in Cerebral Cortex Following Traumatic Brain Injury in Rats
Yao, X.-L., Liu, J., Lee, E., Ling, G. S. F., & McCabe, J. T. (2005) · Journal of Neurotrauma · doi:10.1089/neu.2005.22.656 · Cited by 112 · see citing works
Role of the Cell Cycle in the Pathobiology of Central Nervous System Trauma
Černak, I., Stoica, B. A., Byrnes, K. R., Giovanni, S. D., & Faden, A. I. (2005) · Cell Cycle · doi:10.4161/cc.4.9.1996 · Cited by 112 · see citing works
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Use of a Poly(ADP-Ribose) Polymerase Inhibitor to Suppress Inflammation and Neuronal Death After Cerebral Ischemia-Reperfusion
Hamby, A. M., Suh, S. W., Kauppinen, T. M., & Swanson, R. A. (2007) · Stroke · doi:10.1161/01.str.0000250742.61241.79 · Cited by 111 · see citing works
Attenuation of acute mitochondrial dysfunction after traumatic brain injury in mice by NIM811, a non-immunosuppressive cyclosporin A analog
Mbye, L. H., Singh, I. N., Sullivan, P. G., Springer, J. E., & Hall, E. D. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.09.025 · Cited by 109 · see citing works
Behavioral Responses of C57BL/6, FVB/N, and 129/SvEMS Mouse Strains to Traumatic Brain Injury: Implications for Gene Targeting Approaches to Neurotrauma
Fox, G. B., LeVasseur, R. A., & Faden, A. I. (1999) · Journal of Neurotrauma · doi:10.1089/neu.1999.16.377 · Cited by 108 · see citing works
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Roscovitine Reduces Neuronal Loss, Glial Activation, and Neurologic Deficits after Brain Trauma
Hilton, G. D., Stoica, B. A., Byrnes, K. R., & Faden, A. I. (2008) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2008.75 · Cited by 108 · see citing works
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Progesterone in the clinical treatment of acute traumatic brain injury
Stein, D. G., & Wright, D. W. (2010) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.2010.489549 · Cited by 108 · see citing works
Neuropathology of the vegetative state after head injury
Graham, D. I., Adams, J., Murray, L. S., & Jennett, B. (2005) · Neuropsychological Rehabilitation · doi:10.1080/09602010443000452 · Cited by 106 · see citing works
Effects of progesterone on neurologic and morphologic outcome following diffuse traumatic brain injury in rats
O'Connor, C. A., Černak, I., JOHNSON, F., & Vink, R. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.01.034 · Cited by 96 · see citing works
Administration of estradiol and progesterone modulate the activities of antioxidant enzyme and aminotransferases in naturally menopausal rats
Moorthy, K., Sharma, D., Basir, S. F., & Baquer, N. Z. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.01.004 · Cited by 96 · see citing works
Neuroprotective effects of novel small peptides in vitro and after brain injury
Faden, A. I., Movsesyan, V. A., Knoblach, S. M., Ahmed, F. A. K. M., & Černak, I. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.04.001 · Cited by 94 · see citing works
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Statins in Traumatic Brain Injury
Wible, E. F., & Laskowitz, D. T. (2010) · Neurotherapeutics · doi:10.1016/j.nurt.2009.11.003 · Cited by 88 · see citing works
Effect of Rosuvastatin on Amnesia and Disorientation after Traumatic Brain Injury (NCT00329758)
Tapia-Pérez, J. H., Sánchez-Aguilar, M., Torres-Corzo, J. G., Gordillo‐Moscoso, A., Martínez-Pérez, P., Madeville, P., Mendoza, E. D. L. C., & Chalita-Williams, J. C. (2008) · Journal of Neurotrauma · doi:10.1089/neu.2008.0554 · Cited by 86 · see citing works
Increase in phosphorylation of Akt and its downstream signaling targets and suppression of apoptosis by simvastatin after traumatic brain injury
Wu, H., Lu, D., Jiang, H., Xiong, Y., Qu, C., Лі, Б., Mahmood, A., Zhou, D., & Chopp, M. (2008) · Journal of neurosurgery · doi:10.3171/jns/2008/109/10/0691 · Cited by 84 · see citing works
Inhibition of Poly(ADP-Ribose) Polymerase Suppresses Inflammation and Promotes Recovery after Ischemic Injury
Kauppinen, T. M., Suh, S. W., Berman, A., Hamby, A. M., & Swanson, R. A. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.9 · Cited by 84 · see citing works
Novel Diketopiperazine Enhances Motor and Cognitive Recovery After Traumatic Brain Injury in Rats and Shows Neuroprotection In Vitro and In Vivo
Faden, A. I., Knoblach, S. M., Černak, I., Fan, L., Vink, R., Araldi, G. L., Fricke, S. T., Roth, B. L., & Kozikowski, A. P. (2003) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/01.wcb.0000046143.31247.fd · Cited by 77 · see citing works
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Basis of progesterone protection in spinal cord neurodegeneration
Deniselle, M. C. G., Costa, J. J. L., González, S. L., Labombarda, F., Garay, L. I., Guennoun, R., Schumacher, M., & Nicola, A. F. D. (2002) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(02)00262-5 · Cited by 77 · see citing works
Inhibitory effect of progesterone on inflammatory factors after experimental traumatic brain injury.
Pan, D.-S., Liu, W., Yang, X., & Cao, F. (2007) · PubMed · Cited by 73 · see citing works
Brain metabolic and hemodynamic effects of cyclosporin A after human severe traumatic brain injury: a microdialysis study
Mazzeo, A. T., Alves, O. L., Gilman, C. B., Hayes, R. L., Tolias, C. M., Kunene, K. N., & Bullock, M. R. (2008) · Acta Neurochirurgica · doi:10.1007/s00701-008-0021-7 · Cited by 72 · see citing works
Drugs acting on SUR1 to treat CNS ischemia and trauma
Simard, J. M., WOO, S., Bhatta, S., & Gerzanich, V. (2007) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2007.10.004 · Cited by 62 · see citing works
Effect of atorvastatin on spatial memory, neuronal survival, and vascular density in female rats after traumatic brain injury
Qu, C., Lu, D., Goussev, A. V., Schallert, T. J., Mahmood, A., & Chopp, M. (2005) · Journal of neurosurgery · doi:10.3171/jns.2005.103.4.0695 · Cited by 62 · see citing works
Substance P Antagonists as a Therapeutic Approach to Improving Outcome Following Traumatic Brain Injury
Vink, R., & van den Heuvel, C. (2010) · Neurotherapeutics · doi:10.1016/j.nurt.2009.10.018 · Cited by 56 · see citing works
Local Administration of the Poly(ADP-Ribose) Polymerase Inhibitor INO-1001 Prevents NAD + Depletion and Improves Water Maze Performance after Traumatic Brain Injury in Mice
Clark, R. S. B., Vagni, V., Nathaniel, P. D., Jenkins, L. W., Dixon, C. E., & Szabó, C. (2007) · Journal of Neurotrauma · doi:10.1089/neu.2007.0305 · Cited by 56 · see citing works
Peripheral administration of a novel diketopiperazine, NNZ 2591, prevents brain injury and improves somatosensory-motor function following hypoxia–ischemia in adult rats
Guan, J., Mathai, S., Harris, P. W. R., Wen, J., Zhang, R., Brimble, M. A., & Gluckman, P. D. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.08.010 · Cited by 52 · see citing works
Intracellular progesterone receptors are differentially regulated by sex steroid hormones in the hypothalamus and the cerebral cortex of the rabbit
Camacho‐Arroyo, I., Pérez‐Palacios, G., Pasapera, A. M., & Cerbón, M. (1994) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/0960-0760(94)90135-x · Cited by 48 · see citing works
Multifunctional Drug Treatment in Neurotrauma
Stoica, B. A., Byrnes, K. R., & Faden, A. I. (2008) · Neurotherapeutics · doi:10.1016/j.nurt.2008.10.029 · Cited by 47 · see citing works
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Effects of progesterone on experimental spinal cord injury
Fee, D. B., Swartz, K. R., Joy, K. M., Roberts, K. N., Scheff, N. N., & Scheff, S. W. (2007) · Brain Research · doi:10.1016/j.brainres.2006.12.024 · Cited by 45 · see citing works
Neuroprotective and Nootropic Actions of a Novel Cyclized Dipeptide After Controlled Cortical Impact Injury in Mice
Faden, A. I., Fox, G. B., Di, X., Knoblach, S. M., Černak, I., Mullins, P. G., Nikolaeva, M. A., & Kozikowski, A. P. (2003) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/01.wcb.0000046144.31247.33 · Cited by 44 · see citing works
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Inhibition of Cell Cycle Pathway by Flavopiridol Promotes Survival of Cerebellar Granule Cells after an Excitotoxic Treatment
Verdaguer, E., Jiménez, A., Canudas, A. M., Jordà, E. G., Sureda, F. X., Pallàs, M., & Camins, A. (2004) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.057497 · Cited by 43 · see citing works
Efficacy of Progesterone following a Moderate Unilateral Cortical Contusion Injury
Gilmer, L. K., Roberts, K. N., & Scheff, S. (2008) · Journal of Neurotrauma · doi:10.1089/neu.2007.0477 · Cited by 40 · see citing works
Novel small peptides with neuroprotective and nootropic properties
Faden, A. I., Knoblach, S. M., Movsesyan, V. A., & Černak, I. (2005) · Journal of Alzheimer s Disease · doi:10.3233/jad-2004-6s603 · Cited by 38 · see citing works
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boc-Aspartyl(OMe)-Fluoromethylketone Attenuates Mitochondrial Release of Cytochrome c and Delays Brain Tissue Loss after Traumatic Brain Injury in Rats
Clark, R. S. B., Nathaniel, P. D., Zhang, X., Dixon, C. E., Alber, S. M., Watkins, S. C., Melick, J. A., Kochanek, P. M., & Graham, S. H. (2006) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600338 · Cited by 38 · see citing works
Inhibitory Effect of Progesterone on Inflammatory Factors After Experimental Traumatic Brain Injury
Sheng, P. (2007) · 生物医学与环境科学：英文版 · Cited by 34 · see citing works
Statins and neuroprotection
Sheehy, N. P., Vaughan, C. J., & Delanty, N. (2001) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.10.10.1847 · Cited by 31 · see citing works
Novel Neuroprotective Tripeptides and Dipeptides
Faden, A. I., Knoblach, S. M., Movsesyan, V. A., Lea, P. M., & Černak, I. (2005) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2005.tb00057.x · Cited by 27 · see citing works
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Combination therapies for traumatic brain injury: prospective considerations
Margulies, S. S., & Hicks, R. (2009) · Journal of Neurotrauma · doi:10.1089/neu.2008-0794 · Cited by 22 · see citing works
Novel Neuroprotective Tripeptides and Dipeptides
Faden, A. I. (2005) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1344.041 · Cited by 17 · see citing works
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Animal models of traumatic brain injury
Xiong, Y., Mahmood, A., & Chopp, M. (2013) · Nature reviews. Neuroscience · doi:10.1038/nrn3407 · Cited by 1,413 · see citing works
Neuroinflammation after traumatic brain injury: Opportunities for therapeutic intervention
Kumar, A., & Loane, D. J. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.06.008 · Cited by 684 · see citing works
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Very Early Administration of Progesterone for Acute Traumatic Brain Injury
Wright, D. W., Yeatts, S. D., Silbergleit, R., Palesch, Y. Y., Hertzberg, V. S., Frankel, M., Goldstein, F. C., Caveney, A. F., Howlett-Smith, H., Bengelink, E. M., et al. (2014) · New England Journal of Medicine · doi:10.1056/nejmoa1404304 · Cited by 567 · see citing works
Long-Term Consequences of Traumatic Brain Injury: Current Status of Potential Mechanisms of Injury and Neurological Outcomes
Bramlett, H. M., & Dietrich, W. D. (2014) · Journal of Neurotrauma · doi:10.1089/neu.2014.3352 · Cited by 554 · see citing works
Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know
Gupte, R. P., Brooks, W. M., Vukas, R. R., Pierce, J. D., & Harris, J. L. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.6171 · Cited by 533 · see citing works
Neuroimaging after mild traumatic brain injury: review and meta-analysis
Eierud, C., Craddock, R. C., Fletcher, S., Aulakh, M., King-Casas, B., Kuehl, D., & LaConte, S. M. (2014) · NeuroImage: Clinical · doi:10.1016/j.nicl.2013.12.009 · Cited by 524 · see citing works
Progressive Neurodegeneration After Experimental Brain Trauma: Association With Chronic Microglial Activation
Loane, D. J., Kumar, A., Stoica, B. A., Cabatbat, R., & Faden, A. I. (2014) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0000000000000021 · Cited by 498 · see citing works
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Microglial Activation in Traumatic Brain Injury
Donat, C. K., Scott, G., Gentleman, S., & Sastre, M. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00208 · Cited by 489 · see citing works
Neuroinflammatory responses to traumatic brain injury: etiology, clinical consequences, and therapeutic opportunities
Borlongan, C. V., Acosta, S., de la Peña, I., Tajiri, N., Kaneko, Y., Lozano, D., & Gonzales-Portillo, G. S. (2015) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s65815 · Cited by 415 · see citing works
HDAC inhibition prevents white matter injury by modulating microglia/macrophage polarization through the GSK3β/PTEN/Akt axis
Wang, G., Shi, Y., Jiang, X., Leak, R. K., Hu, X., Wu, Y., Pu, H., Li, W.-W., Tang, B., Wang, Y., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1501441112 · Cited by 376 · see citing works
Mer regulates microglial/macrophage M1/M2 polarization and alleviates neuroinflammation following traumatic brain injury
Wu, H., Zheng, J., Xu, S., Fang, Y., Wu, Y., Zeng, J., Shao, A., Shi, L., Lü, J., Mei, S., et al. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-020-02041-7 · Cited by 350 · see citing works
Microglial Depletion with CSF1R Inhibitor During Chronic Phase of Experimental Traumatic Brain Injury Reduces Neurodegeneration and Neurological Deficits
Henry, R. J., Ritzel, R. M., Barrett, J. P., Doran, S. J., Jiao, Y., Leach, J. B., Szeto, G. L., Wu, J., Stoica, B. A., Faden, A. I., et al. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2402-19.2020 · Cited by 333 · see citing works
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Impaired autophagy flux is associated with neuronal cell death after traumatic brain injury
Sarkar, C., Zhao, Z., Aungst, S. L., Sabirzhanov, B. E., Faden, A. I., & Lipinski, M. M. (2014) · Autophagy · doi:10.4161/15548627.2014.981787 · Cited by 327 · see citing works
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Microglial-derived microparticles mediate neuroinflammation after traumatic brain injury
Kumar, A., Stoica, B. A., Loane, D. J., Yang, M., Abulwerdi, G. A., Khan, N., Kumar, A., Thom, S. R., & Faden, A. I. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0819-4 · Cited by 318 · see citing works
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Mitochondrial dysfunction and oxidative stress in Alzheimer’s disease, and Parkinson’s disease, Huntington’s disease and Amyotrophic Lateral Sclerosis -An updated review
Alqahtani, T., Deore, S. L., Kide, A. A., Shende, B. A., Sharma, R., Chakole, R. D., Nemade, L. S., Kale, N. K., Borah, S., Deokar, S. S., et al. (2023) · Mitochondrion · doi:10.1016/j.mito.2023.05.007 · Cited by 289 · see citing works
Photobiomodulation for traumatic brain injury and stroke
Hamblin, M. R. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.24190 · Cited by 259 · see citing works
Traumatic brain injury: pathophysiology for neurocritical care
Kinoshita, K. (2016) · Journal of Intensive Care · doi:10.1186/s40560-016-0138-3 · Cited by 257 · see citing works
Animal modelling of traumatic brain injury in preclinical drug development: where do we go from here?
Marklund, N., & Hillered, L. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.01163.x · Cited by 254 · see citing works
Chronic Neurodegeneration After Traumatic Brain Injury: Alzheimer Disease, Chronic Traumatic Encephalopathy, or Persistent Neuroinflammation?
Faden, A. I., & Loane, D. J. (2015) · Neurotherapeutics · doi:10.1007/s13311-014-0319-5 · Cited by 245 · see citing works
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Animal tests for anxiety-like and depression-like behavior in rats
Belovičová, K., Bögi, E., Csatlósová, K., & Dubovický, M. (2017) · Interdisciplinary Toxicology · doi:10.1515/intox-2017-0006 · Cited by 244 · see citing works
Current understanding of neuroinflammation after traumatic brain injury and cell-based therapeutic opportunities
Xiong, Y., Mahmood, A., & Chopp, M. (2018) · Chinese Journal of Traumatology · doi:10.1016/j.cjtee.2018.02.003 · Cited by 237 · see citing works
MSCs-Derived Exosomes and Neuroinflammation, Neurogenesis and Therapy of Traumatic Brain Injury
Yang, Y., Ye, Y., Su, X., He, J., Bai, W., & He, X. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00055 · Cited by 236 · see citing works
Brain-gut axis dysfunction in the pathogenesis of traumatic brain injury
Hanscom, M., Loane, D. J., & Shea‐Donohue, T. (2021) · Journal of Clinical Investigation · doi:10.1172/jci143777 · Cited by 233 · see citing works
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Revisiting Traumatic Brain Injury: From Molecular Mechanisms to Therapeutic Interventions
Jarrahi, A., Braun, M., Ahluwalia, M., Gupta, R. V., Wilson, M., Munie, S., Ahluwalia, P. K., Vender, J. R., Vale, F. Ĺ., Dhandapani, K. M., et al. (2020) · Biomedicines · doi:10.3390/biomedicines8100389 · Cited by 226 · see citing works
Repeated Mild Traumatic Brain Injury
Fehily, B., & Fitzgerald, M. (2017) · Cell Transplantation · doi:10.1177/0963689717714092 · Cited by 223 · see citing works
Function and Mechanisms of Autophagy in Brain and Spinal Cord Trauma
Lipinski, M. M., Wu, J., Faden, A. I., & Sarkar, C. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2015.6306 · Cited by 221 · see citing works
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NOX2 drives M1-like microglial/macrophage activation and neurodegeneration following experimental traumatic brain injury
Kumar, A., Barrett, J. P., Alvarez-Croda, D.-M., Stoica, B. A., Faden, A. I., & Loane, D. J. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.07.158 · Cited by 213 · see citing works
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Studies of selective TNF inhibitors in the treatment of brain injury from stroke and trauma: a review of the evidence to date
Tuttolomondo, A., Pecoraro, R., & Pinto, A. V. (2014) · Drug Design Development and Therapy · doi:10.2147/dddt.s67655 · Cited by 208 · see citing works
Structured evaluation of rodent behavioral tests used in drug discovery research
Hånell, A., & Marklund, N. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00252 · Cited by 188 · see citing works
PLA2G4A/cPLA2-mediated lysosomal membrane damage leads to inhibition of autophagy and neurodegeneration after brain trauma
Sarkar, C., Jones, J. W., Hegdekar, N., Thayer, J. A., Kumar, A., Faden, A. I., Kane, M. A., & Lipinski, M. M. (2019) · Autophagy · doi:10.1080/15548627.2019.1628538 · Cited by 188 · see citing works
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Cell Death and Recovery in Traumatic Brain Injury
Akamatsu, Y., & Hanafy, K. A. (2020) · Neurotherapeutics · doi:10.1007/s13311-020-00840-7 · Cited by 187 · see citing works
Late exercise reduces neuroinflammation and cognitive dysfunction after traumatic brain injury
Piao, C.-S., Stoica, B. A., Wu, J., Sabirzhanov, B. E., Zhao, Z., Cabatbat, R. M., Loane, D. J., & Faden, A. I. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.12.017 · Cited by 178 · see citing works
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Delayed mGluR5 activation limits neuroinflammation and neurodegeneration after traumatic brain injury
Byrnes, K. R., Loane, D. J., Stoica, B. A., Zhang, J., & Faden, A. I. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-43 · Cited by 171 · see citing works
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Neuroinflammation in traumatic brain injury: A chronic response to an acute injury
Lozano, D., Schimmel, S. J., & Acosta, S. (2017) · Brain Circulation · doi:10.4103/bc.bc_18_17 · Cited by 173 · see citing works
Neuroprotective Strategies for Traumatic Brain Injury: Improving Clinical Translation
Kabadi, S. V., & Faden, A. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms15011216 · Cited by 183 · see citing works
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Targeting Mitochondrial Dysfunction and Oxidative Stress in Activated Microglia using Dendrimer-Based Therapeutics
Sharma, A., Liaw, K., Sharma, R. B., Zhang, Z., Kannan, S., & Kannan, R. M. (2018) · Theranostics · doi:10.7150/thno.29039 · Cited by 165 · see citing works
Dual effects of carbon monoxide on pericytes and neurogenesis in traumatic brain injury
Choi, Y. K., Maki, T., Mandeville, E. T., Koh, S., Hayakawa, K., Arai, K., Kim, Y., Whalen, M. J., Xing, C., Wang, X., et al. (2016) · Nature Medicine · doi:10.1038/nm.4188 · Cited by 158 · see citing works
Mesenchymal Stem Cell-Derived Exosomes Provide Neuroprotection and Improve Long-Term Neurologic Outcomes in a Swine Model of Traumatic Brain Injury and Hemorrhagic Shock
Williams, A. M., Dennahy, I. S., Bhatti, U. F., Halaweish, I. F., Xiong, Y., Chang, P., Nikolian, V. C., Chtraklin, K., Brown, J. F., Zhang, Y., et al. (2018) · Journal of Neurotrauma · doi:10.1089/neu.2018.5711 · Cited by 158 · see citing works
Novel drug delivery systems for glaucoma
Lavik, E., Kuehn, M. H., & Kwon, Y. H. (2011) · Eye · doi:10.1038/eye.2011.82 · Cited by 157 · see citing works
Inhibition of autophagy in microglia and macrophages exacerbates innate immune responses and worsens brain injury outcomes
Hegdekar, N., Sarkar, C., Bustos, S., Ritzel, R. M., Hanscom, M., Ravishankar, P., Philkana, D., Wu, J., Loane, D. J., & Lipinski, M. M. (2023) · Autophagy · doi:10.1080/15548627.2023.2167689 · Cited by 158 · see citing works
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Transcranial low-level laser therapy enhances learning, memory, and neuroprogenitor cells after traumatic brain injury in mice
Xuan, W., Vatansever, F., Huang, L., & Hamblin, M. R. (2014) · Journal of Biomedical Optics · doi:10.1117/1.jbo.19.10.108003 · Cited by 156 · see citing works
Bone Marrow Mesenchymal Stromal Cells Drive Protective M2 Microglia Polarization After Brain Trauma
Zanier, E. R., Pischiutta, F., Riganti, L., Marchesi, F., Turola, E., Fumagalli, S., Perego, C., Parotto, E., Vinci, P., Veglianese, P., et al. (2014) · Neurotherapeutics · doi:10.1007/s13311-014-0277-y · Cited by 155 · see citing works
Neuroprotection in acute brain injury: an up-to-date review
Stocchetti, N., Taccone, F. S., Citerio, G., Pepe, P. E., Roux, P. D. L., Oddo, M., Polderman, K. H., Stevens, R. D., Barsan, W. G., Maas, A. I. R., et al. (2015) · Critical Care · doi:10.1186/s13054-015-0887-8 · Cited by 157 · see citing works
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STAT1 drives M1 microglia activation and neuroinflammation under hypoxia
Butturini, E., Boriero, D., de Prati, A. C., & Mariotto, S. (2019) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2019.05.011 · Cited by 153 · see citing works
The Role of Neurogenic Inflammation in Blood-Brain Barrier Disruption and Development of Cerebral Oedema Following Acute Central Nervous System (CNS) Injury
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Authors: Loane, D. J., & Faden, A. I.
Affiliations: University of Maryland, Baltimore (US)
Corresponding author: Faden, Alan I.
ORCID: Loane, David J.
Faden, Alan I.
Venue: Trends in Pharmacological Sciences
Publisher: Elsevier BV
Published: 2010-12
Volume: 31
Issue: 12
Pages: 596-604
ISSN: 0165-6147 (ISSN-L)
DOI: 10.1016/j.tips.2010.09.005
PMC: PMC2999630
OpenAlex: W2073814752
Cited by: 574
References: 118
Citations by year: 2026: 19 · 2025: 16 · 2024: 46 · 2023: 24 · 2022: 27 · 2021: 47 · 2020: 51 · 2019: 34 · 2018: 42 · 2017: 51 · 2016: 41 · 2015: 41 · 2014: 47 · 2013: 36 · 2012: 33
FWCI: 3.53
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Trends in Pharmacological Sciences (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Neurological Disorders and Stroke (R01NS037313, R01NS061839, R01NS052568)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (RC1HD064758)
Topics: Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Automotive and Human Injury Biomechanics
Keywords: traumatic brain injury, neuroprotection, secondary brain injury, neuronal cell death, translational research, clinical trial failure, animal models of TBI, clinical trial design
MeSH terms: Animals, Brain, Brain Injuries, Clinical Trials as Topic, Drug Evaluation, Preclinical, Humans, Nerve Degeneration, Drugs, Investigational, Drug Delivery Systems, Neuroprotective Agents, Translational Research, Biomedical

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Neuroprotection for traumatic brain injury: translational challenges and emerging therapeutic strategies

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