The genetic ablation of tau improves long-term, but not short-term, functional outcomes after experimental traumatic brain injury in mice

References

• Blennow K, Hardy J, Zetterberg H. The neuropathology and neurobiology of traumatic brain injury. Neuron. 2012;76(5):886–99. doi:10.1016/j.neuron.2012.11.021.
   PubMed Web of Science ®Google Scholar
• Xiong Y, Mahmood A, Chopp M. Animal models of traumatic brain injury. Nat Rev Neurosci. 2013;14(2):128–42. doi:10.1038/nrn3407.
   PubMed Web of Science ®Google Scholar
• Johnson VE, Stewart W, Smith DH. Widespread tau and amyloid‐beta pathology many years after a single traumatic brain injury in humans. Brain Pathol. 2012;22(2):142–49. doi:10.1111/j.1750-3639.2011.00513.x.
   PubMed Web of Science ®Google Scholar
• Shultz SR, Wright DK, Zheng P, Stuchbery R, Liu SJ, Sashindranath M, Medcalf RL, Johnston LA, Hoven CM, Jones NC, et al. Sodium selenate reduces hyperphosphorylated tau and improves outcomes after traumatic brain injury. Brain. 2015;138(5):1297–313. doi:10.1093/brain/awv053.
   PubMedGoogle Scholar
• Thom M, Liu JY, Thompson P, Phadke R, Narkiewicz M, Martinian L, Marsdon D, Koepp M, Cabocio L, Catarino CB, et al. Neurofibrillary tangle pathology and Braak staging in chronic epilepsy in relation to traumatic brain injury and hippocampal sclerosis: a post-mortem study. Brain. 2011;134(10):2969–81. doi:10.1093/brain/awr209.
   PubMedGoogle Scholar
• Zheng P, Shultz SR, Hovens CM, Velakoulis D, Jones NC, O’Brien TJ. Hyperphosphorylated tau is implicated in acquired epilepsy and neuropsychiatric comorbidities. Mol Neurobiol. 2014;49(3):1532–39. doi:10.1007/s12035-013-8601-9.
   PubMed Web of Science ®Google Scholar
• Ballatore C, Lee VMY, Trojanowski JQ. Tau-mediated neurodegeneration in Alzheimer’s disease and related disorders. Nat Rev Neurosci. 2007;8(9):663. doi:10.1038/nrn2194.
   PubMed Web of Science ®Google Scholar
• Morris M, Maeda S, Vossel K, Mucke L. The many faces of tau. Neuron. 2011;70(3):410–26. doi:10.1016/j.neuron.2011.04.009.
   PubMed Web of Science ®Google Scholar
• Alonso ADC, Zaidi T, Grundke-Iqbal I, Iqbal K. Role of abnormally phosphorylated tau in the breakdown of microtubules in Alzheimer disease. Proc Natl Acad Sci USA. 1994;91(12):5562–66. doi:10.1073/pnas.91.12.5562.
   PubMed Web of Science ®Google Scholar
• Alonso ADC, Grundke-Iqbal I, Iqbal K. Alzheimer’s disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules. Nat Med. 1996;2(7):783–87.
   PubMed Web of Science ®Google Scholar
• Andrews-Zwilling Y, Bien-Ly N, Xu Q, Li G, Bernardo A, Yoon SY, Zwilling D, Yan TX, Chen L, Huang Y. Apolipoprotein E4 causes age-and Tau-dependent impairment of GABAergic interneurons, leading to learning and memory deficits in mice. J Neurosci. 2010;30(41):13707–17. doi:10.1523/JNEUROSCI.4040-10.2010.
   PubMed Web of Science ®Google Scholar
• Roberson ED, Scearce-Levie K, Palop JJ, Yan F, Cheng IH, Wu T, Gerstein H, Yu GQ, Mucke L. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer’s disease mouse model. Science. 2007;316(5825):750–54. doi:10.1126/science.1141736.
   PubMed Web of Science ®Google Scholar
• Liu SJ, Zheng P, Wright DK, Dezsi G, Braine E, Nguyen T, Corcoran NM, Johnston LA, Hovens CM, Hudson M, et al. Sodium selenate retards epileptogenesis in acquired epilepsy models reversing changes in protein phosphatase 2A and hyperphosphorylated tau. Brain. 2016;139(7):1919–38. doi:10.1093/brain/aww116.
   PubMedGoogle Scholar
• Tan XL, Wright DK, Liu S, Hovens C, O’Brien TJ, Shultz SR. Sodium selenate, a protein phosphatase 2A activator, mitigates hyperphosphorylated tau and improves repeated mild traumatic brain injury outcomes. Neuropharmacology. 2016;108:382–93. doi:10.1016/j.neuropharm.2016.05.001.
   PubMed Web of Science ®Google Scholar
• Lei P, Ayton S, Finkelstein DI, Spoerri L, Ciccotosto GD, Wright DK, Wong BX, Adlard PA, Cherny RA, Lam LQ, et al. Tau deficiency induces parkinsonism with dementia by impairing APP-mediated iron export. Nat Med. 2012;29:291–95.
   Google Scholar
• Liu S, Shen Y, Shultz SR, Nguyen A, Hovens C, Adlard PA, Bush AI, Chan J, Kwan P, O’Brien TJ, et al. Accelerated kindling epileptogenesis in Tg4510 tau transgenic mice, but not in tau knockout mice. Epilepsia. 2017;58(9):e136–2141. doi:10.1111/epi.13847.
   PubMed Web of Science ®Google Scholar
• Johnstone MR, Sun M, Taylor CJ, Brady RD, Grills BL, Church JE, Shultz SR, McDonald SJ. Gambogic amide, a selective TrkA agonist, does not improve outcomes from traumatic brain injury in mice. Brain Inj. 2018;32:257–68. doi:10.1080/02699052.2017.1394492.
   PubMed Web of Science ®Google Scholar
• Shultz SR, Tan XL, Wright DK, Liu SJ, Semple BD, Johnston L, Jones NC, Cook AD, Hamilton JA, O’Brien TJ. Granulocyte-macrophage colony-stimulating factor is neuroprotective in experimental traumatic brain injury. J Neurotrauma. 2014;31(10):976–83. doi:10.1089/neu.2013.3106.
   PubMed Web of Science ®Google Scholar
• Shultz SR, McDonald SJ, Haar CV, Meconi A, Vink R, van Donkelaar P, Taneja C, Iverson GL, Christie BR. The potential for animal models to provide insight into mild traumatic brain injury: translational challenges and strategies. Neurosci Biobehav Rev. 2017;76:396–414. doi:10.1016/j.neubiorev.2016.09.014.
   PubMed Web of Science ®Google Scholar
• Walf AA, Frye CA. The use of the elevated plus maze as an assay of anxiety-related behaviour in rodents. Nat Protoc. 2007;2(2):322–28. doi:10.1038/nprot.2007.44.
   PubMed Web of Science ®Google Scholar
• Sun M, Brady RD, Wright DK, Kim HA, Zhang SR, Sobey CG, Johnstone MR, O’Brien TJ, Semple BD, McDonald SJ, et al. Treatment with an interleukin-1 receptor antagonist mitigates neuroinflammation and brain damage after polytrauma. Brain Behav Immun. 2017;66:359–71. doi:10.1016/j.bbi.2017.08.005.
   PubMed Web of Science ®Google Scholar
• Wright DK, O’Brien TJ, Shultz SR, Mychasiuk R. Sex matters: repetitive mild traumatic brain injury in adolescent rats. Ann Clin Transl Neurol. 2017;4(9):640–54. doi:10.1002/acn3.441.
   PubMed Web of Science ®Google Scholar
• Bortolato M, Godar SC, Davarian S, Chen K, Shih JC. Behavioral disinhibition and reduced anxiety-like behaviors in monoamine oxidase B-deficient mice. Neuropsychopharmacology. 2009;34(13):2746–57. doi:10.1038/npp.2009.118.
   PubMed Web of Science ®Google Scholar
• Lindemann S, Gernert M, Bennay M, Koch M, Löscher W. Comparative analysis of anxiety-like behaviors and sensorimotor functions in two rat mutants, ci2 and ci3, with lateralized rotational behaviour. Physiol Behav. 2008;93(1–2):417–26. doi:10.1016/j.physbeh.2007.11.034.
   PubMed Web of Science ®Google Scholar
• Meyer JS, Piper BJ, Vancollie VE. Development and characterization of a novel animal model of intermittent MDMA (“Ecstasy”) exposure during adolescence. Ann NY Acad Sci. 2008;1139(1):151–63. doi:10.1196/annals.1432.029.
   PubMedGoogle Scholar
• Shultz SR, MacFabe DF, Foley KA, Taylor R, Cain DP. A single mild fluid percussion injury induces short-term behavioural and neuropathological changes in the long–evans rat: support for an animal model of concussion. Behav Brain Res. 2011;224(2):326–35. doi:10.1016/j.bbr.2011.06.012.
   PubMed Web of Science ®Google Scholar
• Bao F, Shultz SR, Hepburn JD, Omana V, Weaver LC, Cain DP, Brown A. A CD11d monoclonal antibody treatment reduces tissue injury and improves neurological outcome after fluid percussion brain injury in rats. J Neurotrauma. 2012;29(14):2375–92. doi:10.1089/neu.2012.2408.
   PubMed Web of Science ®Google Scholar
• Johnstone VP, Wright DK, Wong K, O’Brien TJ, Rajan R, Shultz SR. Experimental traumatic brain injury results in long-term recovery of functional responsiveness in sensory cortex but persisting structural changes and sensorimotor, cognitive, and emotional deficits. J Neurotrauma. 2015;32(17):1333–46. doi:10.1089/neu.2014.3785.
   PubMed Web of Science ®Google Scholar
• Jones NC, Cardamone L, Williams JP, Salzberg MR, Myers D, O’Brien TJ. Experimental traumatic brain injury induces a pervasive hyperanxious phenotype in rats. J Neurotrauma. 2008;25(11):1367–74. doi:10.1089/neu.2008.0641.
   PubMed Web of Science ®Google Scholar
• Shultz SR, McDonald SJ, Corrigan F, Semple BD, Salberg S, Zamani A, Jones NC, Mychasiuk R. The clinical relevance of behavior testing in animal models of traumatic brain injury. J Neurotrauma. 2019. doi:10.1089/neu.2018.6149.
   Google Scholar
• Semple BD, Zamani A, Rayner G, Shultz SR, Jones NC. Affective, neurocognitive and psychosocial disorders associated with traumatic brain injury and post-traumatic epilepsy. Neurobiol Dis. 2019;123:27–41. doi:10.1016/j.nbd.2018.07.018.
   PubMed Web of Science ®Google Scholar
• Fan LW, Tien LT, Mitchell HJ, Rhodes PG, Cai Z. α‐Phenyl‐n‐tert‐butyl‐nitrone ameliorates hippocampal injury and improves learning and memory in juvenile rats following neonatal exposure to lipopolysaccharide. Eur J Neurosci. 2008;7(6):1475–84. doi:10.1111/j.1460-9568.2008.06121.x.
   Google Scholar
• Shultz SR, Cardamone L, Liu YR, Hogan RE, Maccotta L, Wright DK, Zheng P, Koe A, Gregoire MC, Williams JP, et al. Can structural or functional changes following traumatic brain injury in the rat predict epileptic outcome? Epilepsia. 2013;54(7):1240–50. doi:10.1111/epi.12223.
   PubMed Web of Science ®Google Scholar
• Cheng JS, Craft R, Yu GQ, Ho K, Wang X, Mohan G, Mangnitsky S, Ponnusamy R, Mucke L. Tau reduction diminishes spatial learning and memory deficits after mild repetitive traumatic brain injury in mice. PLoS One. 2014;9(12):e115765. doi:10.1371/journal.pone.0115765.
   PubMed Web of Science ®Google Scholar
• Collins-Praino LE, Corrigan F. Does neuroinflammation drive the relationship between tau hyperphosphorylation and dementia development following traumatic brain injury. Brain Behav Immun. 2017;60:369–82. doi:10.106/j.bbi.2016.09.027.
   Google Scholar