Traumatic brain injury: Recent advances in plasticity and regeneration

Current Opinion in Neurology

Volumn 28, Issue 6, 2015, Pages 565-573

  Werner, J Kent ^a   Stevens, Robert D ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Biomarkers; Exosomes; Plasticity; Regeneration; Stem cells; Traumatic brain injury

Indexed keywords

BIOLOGICAL MARKER; CYCLOSERINE; CYCLOSPORIN A; MINOCYCLINE; NEUROTROPHIC FACTOR; SEROTONIN; SIMVASTATIN; TOPIRAMATE; TROFINETIDE; VALPROIC ACID;

APOPTOSIS; AUTOLOGOUS BONE MARROW TRANSPLANTATION; BLOOD BRAIN BARRIER; CELL COMMUNICATION; CELL DEATH; CELL POPULATION; CELL THERAPY; CENTRAL NERVOUS SYSTEM; CLINICAL EFFECTIVENESS; CYTOSKELETON; ENVIRONMENTAL ENRICHMENT; EXOSOME; HUMAN; HYPERBARIC OXYGEN; IMMUNE RESPONSE; MECHANOTRANSDUCTION; NERVE CELL PLASTICITY; NERVE REGENERATION; NEURAL STEM CELL; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; PATIENT SAFETY; PROGNOSIS; PROTEIN EXPRESSION; RECREATION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL NICHE; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRAUMATIC BRAIN INJURY; BRAIN INJURIES; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

BRAIN INJURIES; EXOSOMES; HUMANS; NERVE REGENERATION; NEURONAL PLASTICITY; SIGNAL TRANSDUCTION;

EID: 84947493765     PISSN: 13507540     EISSN: 14736551     Source Type: Journal    
DOI: 10.1097/WCO.0000000000000265     Document Type: Review

References (95)

1. Faul M, Coronado V. Epidemiology of traumatic brain injury. Handb Clin Neurol 2015; 127:3-13.
2. Clifton GL, Valadka A, Zygun D, et al. Very early hypothermia induction in patients with severe brain injury (the National Acute Brain Injury Study: Hypothermia II): a randomised trial. Lancet Neurol 2011; 10:131-139.
3. Edwards P, Arango M, Balica L, et al. Final results of MRC CRASH, a randomised placebo-controlled trial of intravenous corticosteroid in adults with head injury-outcomes at 6 months. Lancet 2005; 365:1957-1959.
4. Maas AI, Murray G, Henney H 3rd, et al. Efficacy and safety of dexanabinol in severe traumatic brain injury: results of a phase III randomised, placebo-controlled, clinical trial. Lancet Neurol 2006; 5:38-45.
5. Zafonte RD, Bagiella E, Ansel BM, et al. Effect of citicoline on functional and cognitive status among patients with traumatic brain injury: Citicoline Brain Injury Treatment Trial (COBRIT). JAMA 2012; 308:1993-2000.
6. Robertson CS, Hannay HJ, Yamal J-M, et al. Effect of erythropoietin and transfusion threshold on neurological recovery after traumatic brain injury: a randomized clinical trial. JAMA 2014; 312:36-47.
7. Wright DW, Yeatts SD, Silbergleit R, et al. Very early administration of progesterone for acute traumatic brain injury. N Engl J Med 2014; 371:2457-2466.
8. Skolnick BE, Maas AI, Narayan RK, et al. A clinical trial of progesterone for severe traumatic brain injury. N Engl J Med 2014; 371:2467-2476.
9. Sharp DJ, Scott G, Leech R. Network dysfunction after traumatic brain injury. Nat Rev Neurol 2014; 10:156-166.
10. Burda JE, Bernstein AM, Sofroniew MV. Astrocyte roles in traumatic brain injury. Exp Neurol 2015. [Epub ahead of print]
11. Blennow K, Hardy J, Zetterberg H. The neuropathology and neurobiology of traumatic brain injury. Neuron 2012; 76:886-899.
12. Hemphill Matthew A, Dauth S, Yu Chung J, et al. Traumatic Brain Injury and the neuronal microenvironment: a potential role for neuropathological mechan-otransduction. Neuron 2015; 85:1177-1192.
13. Corps KN, Roth TL, McGavern DB. Inflammation and neuroprotection in traumatic brain injury. JAMA Neurol 2015; 72:355-362.
14. Plesnila N, von Baumgarten L, Retiounskaia M, et al. Delayed neuronal death after brain trauma involves p53-dependent inhibition of NF-kappa B transcrip-tional activity. Cell Death Differ 2007; 14:1529-1541.
15. Nieto-Sampedro M, Lewis ER, Cotman CW, et al. Brain injury causes a time-dependent increase in neuronotrophic activity at the lesion site. Science 1982; 217:860-861.
16. Massa SM, Yang T, Xie Y, et al. Small molecule BDNF mimetics activate TrkB signaling and prevent neuronal degeneration in rodents. J Clin Invest 2010; 120:1774-1785.
17. Chiaretti A, Barone G, Riccardi R, et al. NGF, DCX, and NSE upregulation correlates with severity and outcome of head trauma in children. Neurology 2009; 72:609-616.
18. Chiaretti A, Piastra M, Polidori G, et al. Correlation between neurotrophic factor expression and outcome of children with severe traumatic brain injury. Intensive Care Med 2003; 29:1329-1338.
19. Blaha GR, Raghupathi R, Saatman KE, McIntosh TK. Brain-derived neuro-trophic factor administration after traumatic brain injury in the rat does not protect against behavioral or histological deficits. Neuroscience 2000; 99:483-493.
20. Conte V, Raghupathi R, Watson DJ, et al. TrkB gene transfer does not alter hippocampal neuronal loss and cognitive deficits following traumatic brain injury in mice. Restor Neurol Neurosci 2008; 26:45-56.
21. Failla MD, Kumar RG, Peitzman AB, et al. Variation in the BDNF gene interacts with age to predict mortality in a prospective, longitudinal cohort with severe TBI. Neurorehabil Neural Repair 2015; 29:234-246.
22. Ritter C, Miranda AS, Giombelli VR, et al. Brain-derived neurotrophic factor plasma levels are associated with mortality in critically ill patients even in the absence of brain injury. Crit Care 2012; 16:R234.
23. Failla MD, Conley YP, Wagner AK. Brain-derived neurotrophic factor (BDNF) in traumatic brain injury-related mortality: interrelationships between genetics and acute systemic and central nervous system BDNF profiles. Neurorehabil Neural Repair 2015. [Epub ahead of print]
24. Korley FK, Diaz-Arrastia R, Wu AH, et al. Circulating brain derived neuro-trophic factor (BDNF) has diagnostic and prognostic value in traumatic brain injury. J Neurotrauma 2015. [Epub ahead of print]
25. Kyritsis N, Kizil C, Zocher S, et al. Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 2012; 338:1353-1356.
26. Frank MG, Weber MD, Watkins LR, Maier SF. Stress sounds the alarmin: the role of the danger-associated molecular pattern HMGB1 in stress-induced neuroinflammatory priming. Brain Behav Immun 2015; 48:1-7.
27. Laird MD, Shields JS, Sukumari-Ramesh S, et al. High mobility group box protein-1 promotes cerebral edema after traumatic brain injury via activation of toll-like receptor 4. Glia 2014; 62:26-38.
28. Jayakumar AR, Tong XY, Ruiz-Cordero R, et al. Activation of NF-kappa B mediates astrocyte swelling and brain edema in traumatic brain injury. J Neurotrauma 2014; 31:1249-1257.
29. Addington CP, Roussas A, Dutta D, Stabenfeldt SE. Endogenous repair signaling after brain injury and complementary bioengineering approaches to enhance neural regeneration. Biomark Insights 2015; 10:43-60.
30. Smith ED, Prieto GA, Tong L, et al. Rapamycin and interleukin-1 beta impair brain-derived neurotrophic factor-dependent neuron survival by modulating autophagy. J Biol Chem 2014; 289:20615-20629.
31. Sebastiani A, Golz C, Werner C, et al. Proneurotrophin binding to P75 neurotrophin receptor (P75ntr) is essential for brain lesion formation and functional impairment after experimental traumatic brain injury. J Neurotrauma 2015; 32:1599-1607.
32. Lee C, Agoston DV. Vascular endothelial growth factor is involved in mediating increased de novo hippocampal neurogenesis in response to traumatic brain injury. J Neurotrauma 2010; 27:541-553.
33. Lee R, Kermani P, Teng KK, Hempstead BL. Regulation of cell survival by secreted proneurotrophins. Science 2001; 294:1945-1948.
34. Maya Vetencourt JF, Sale A, Viegi A, et al. The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 2008; 320:385-388.
35. McCann SK, Irvine C, Mead GE, et al. Efficacy of antidepressants in animal models of ischemic stroke: a systematic review and meta-analysis. Stroke 2014; 45:3055-3063.
36. Mead GE, Hsieh CF, Lee R, et al. Selective serotoninre up take in hibitors for stroke recovery:asystematic review and meta-analysis. Stroke 2013; 44:844-850.
37. Santarelli L, Saxe M, Gross C, et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003; 301:805-809.
38. Encinas JM, Vaahtokari A, Enikolopov G. Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci USA 2006; 103:8233-8238.
39. Wang JW, David DJ, Monckton JE, et al. Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J Neurosci 2008; 28:1374-1384.
40. Kobayashi K, Ikeda Y, Sakai A, et al. Reversal of hippocampal neuronal maturation by serotonergic antidepressants. Proc Natl Acad Sci USA 2010; 107:8434-8439.
41. Tong CK, Chen J, Cebrián-Silla A, et al. Axonal control of the adult neural stem cell niche. Cell Stem Cell 2014; 14:500-511.
42. Chollet F, Tardy J, Albucher J-F, et al. Fluoxetine for motor recovery after acute ischaemic stroke (FLAME): a randomised placebo-controlled trial. Lancet Neurol 2011; 10:123-130.
43. Banos JH, Novack TA, Brunner R, et al. Impact of early administration of sertraline on cognitive and behavioral recovery in the first year after moderate to severe traumatic brain injury. J Head Trauma Rehabil 2010; 25:357-361.
44. Wang Y, Neumann M, Hansen K, et al. Fluoxetine increases hippocampal neurogenesis and induces epigenetic factors but does not improve functional recovery after traumatic brain injury. J Neurotrauma 2011; 28:259-268.
45. McAllister BB, Spanswick SC, Patel PP, et al. The effects of chronic fluoxetine treatment following injury of medial frontal cortex in mice. Behav Brain Res 2015; 290:102-116.
46. Harris NG, Chen S-F, Pickard JD. Cortical reorganization after experimental traumatic brain injury: a functional autoradiography study. J Neurotrauma 2013; 30:1137-1146.
47. Jones TA, Liput DJ, Maresh EL, et al. Use-dependent dendritic regrowth is limited after unilateral controlled cortical impact to the forelimb sensorimotor cortex. J Neurotrauma 2012; 29:1455-1468.
48. Sale A, Berardi N, Maffei L. Enrich the environment to empower the brain. Trends Neurosci 2009; 32:233-239.
49. Bondi CO, Klitsch KC, Leary JB, Kline AE. Environmental enrichment as a viable neurorehabilitation strategy for experimental traumatic brain injury. J Neurotrauma 2014; 31:873-888.
50. Greifzu F, Pielecka-Fortuna J, Kalogeraki E, et al. Environmentalenrichmentextends ocular dominance plasticity into adulthood and protects from stroke-induced impairmentsof plasticity. Proc Natl Acad Sci USA 2014; 111:1150-1155.
51. Johnson EM, Traver KL, Hoffman SW, et al. Environmental enrichment protects against functional deficits caused by traumatic brain injury. Front Behav Neurosci 2013; 7:44.
52. Cheng JP, Shaw KE, Monaco CM, et al. A relatively brief exposure to environmental enrichment after experimental traumatic brain injury confers long-term cognitive benefits. J Neurotrauma 2012; 29:2684-2688.
53. Bergami M, Masserdotti G, Temprana SG, et al. A critical period for experience-dependent remodeling of adult-born neuron connectivity. Neuron 2015; 85:710-717.
54. Birch AM, McGarry NB, Kelly AM. Short-term environmental enrichment, inthe absence of exercise, improves memory, and increases NGF concentration, early neuronal survival, and synaptogenesis in the dentate gyrus in a time-dependent manner. Hippocampus 2013; 23:437-450.
55. Goshen I, Avital A, Kreisel T, et al. Environmental enrichment restores memory functioning in mice with impaired IL-1 signaling via reinstatement of long-term potentiation and spine size enlargement. J Neurosci 2009; 29:3395-3403.
56. Young J, Pionk T, Hiatt I, et al. Environmental enrichment aides in functional recovery following unilateral controlled cortical impact of the forelimb sensor-imotor area however intranasal administration of nerve growth factor does not. Brain Res Bull 2015; 115:17-22.
57. Pusic AD, Kraig RP. Youth and environmental enrichment generate serum exosomes containing miR-219 that promote CNS myelination. Glia 2014; 62:284-299.
58. Rajendran L, Bali J, Barr MM, et al. Emerging roles of extracellular vesicles in the nervous system. J Neurosci 2014; 34:15482-15489.
59. Lachenal G, Pernet-Gallay K, Chivet M, et al. Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity. Mol Cell Neurosci 2011; 46:409-418.
60. Chivet M, Javalet C, Laulagnier K, et al. Exosomes secreted by cortical neurons upon glutamatergic synapse activation specifically interact with neurons. J Extracell Vesicles 2014; 3:24722.
61. Wang S, Cesca F, Loers G, et al. Synapsin I is an oligomannose-carrying glycoprotein, acts as an oligomannose-binding lectin, and promotes neurite outgrowth and neuronal survival when released via glia-derived exosomes. J Neurosci 2011; 31:7275-7290.
62. Komuro Y, Xu G, Bhaskar K, Lamb BT. Human tau expression reduces adult neurogenesis in a mouse model of tauopathy. Neurobiol Aging 2015; 36:2034-2042.
63. Saman S, Lee NCY, Inoyo I, et al. Proteins recruited to exosomes by tau overexpression implicate novel cellular mechanisms linking tau secretion with Alzheimer's disease. J Alzheimers Dis 2014; 40 (Suppl 1):S47-S70.
64. Saman S, Kim W, Raya M, et al. Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease. J Biol Chem 2012; 287:3842-3849.
65. McKee AC, Stern RA, Nowinski CJ, et al. The spectrum of disease in chronic traumatic encephalopathy. Brain 2013; 136:43-64.
66. Kondo A, Shahpasand K, Mannix R, et al. Antibody against early driver of neurodegeneration cis P-tau blocks brain injury and tauopathy. Nature 2015; 523:431-436.
67. Patz S, Trattnig C, Grünbacher G, et al. More than cell dust: microparticles isolated from cerebrospinal fluid of brain injured patients are messengers carrying mRNAs, miRNAs, and proteins. J Neurotrauma 2013; 30:1232-1242.
68. de Rivero Vaccari JP, Brand F 3rd, Adamczak S, et al. Exosome-mediated inflammasome signaling after central nervous system injury. J Neurochem 2015. [Epub ahead of print]
69. Taylor DD, Gercel-Taylor C. Exosome platform for diagnosis and monitoring of traumatic brain injury. Philos Trans R Soc Lond B Biol Sci 2014; 369:; pii:20130503.
70. Zetterberg H, Blennow K. Fluid markers of traumatic brain injury. Mol Cell Neurosci 2015; 66:99-102.
71. Papa L, Mittal MK, Ramirez J, et al. In children and youth with mild and moderate traumatic brain injury GFAP out-performs s100beta in detecting traumatic intracranial lesions on CT. J Neurotrauma 2015. [Epub ahead of print]
72. Vos PE, Lamers KJ, Hendriks JC, et al. Glial and neuronal proteins in serum predict outcome after severe traumatic brain injury. Neurology 2004; 62:1303-1310.
73. Papa L, Silvestri S, Brophy GM, et al. GFAP out-performs S100beta in detecting traumatic intracranial lesions on computed tomography in trauma patients with mild traumatic brain injury and those with extracranial lesions. J Neurotrauma 2014; 31:1815-1822.
74. Wang KKW, Zhang Z, Kobeissy FH. Biomarkers of Brain Injury and Neurological Disorders. Boca Raton: CRC Press Taylor and Francis; 2014; 143-144.
75. Mierzwa AJ, Sullivan GM, Beer LA, et al. Comparison of cortical and white matter traumatic brain injury models reveals differential effects in the sub-ventricular zone and divergent Sonic hedgehog signaling pathways in neuroblasts and oligodendrocyte progenitors. ASN Neuro 2014; 6; pii:1759091414551782.
76. Alagappan D, Ziegler AN, Chidambaram S, et al. Insulin-like growth factor receptor signaling is necessary for epidermal growth factor mediated proliferation of SVZ neural precursors in vitro following neonatal hypoxia-ischemia. Front Neurol 2014; 5:79.
77. Gong D, Hao M, Liu L, et al. Prognostic relevance of circulating endothelial progenitor cells for severe traumatic brain injury. Brain Inj 2012; 26:291-297.
78. Sobrino T, Blanco M, Perez-Mato M, et al. Increased levels of circulating endothelial progenitor cells in patients with ischaemic stroke treated with statins during acute phase. Eur J Neurol 2012; 19:1539-1546.
79. Goldshmit Y, Frisca F, Pinto AR, et al. Fgf2 improves functional recovery-decreasing gliosis and increasing radial glia and neural progenitor cells after spinal cord injury. Brain Behav 2014; 4:187-200.
80. Nichols JE, Niles JA, DeWitt D, et al. Neurogenic and neuro-protective potential of a novel subpopulation of peripheral blood-derived CD133+ ABCG2+CXCR4+ mesenchymal stem cells: development of autologous cell-based therapeutics for traumatic brain injury. Stem Cell Res Ther 2013; 4:3.
81. Zheng W, ZhuGe Q, Zhong M, et al. Neurogenesis in adult human brain after traumatic brain injury. J Neurotrauma 2013; 30:1872-1880.
82. Lu KT, Huang TC, Wang JY, et al. NKCC1 mediates traumatic brain injury-induced hippocampal neurogenesis through CREB phosphorylation and HIF-1 alpha expression. Pflugers Arch 2015; 467:1651-1661.
83. Gu YL, Zhang LW, Ma N, et al. Cognitive improvement of mice induced by exercise prior to traumatic brain injury is associated with cytochrome c oxidase. Neurosci Lett 2014; 570:86-91.
84. Agrawal R, Noble E, Tyagi E, et al. Flavonoid derivative 7, 8-DHF attenuates TBI pathology via TrkB activation. Biochim Biophys Acta 2015; 1852:862-872.
85. Oliva AA Jr, Kang Y, Sanchez-Molano J, et al. STAT3 signaling after traumatic brain injury. J Neurochem 2012; 120:710-720.
86. Raible DJ, Frey LC, Del Angel YC, et al. JAK/STAT pathway regulation of GABA receptor expression after differing severities of experimental TBI. Exp Neurol 2015; 271:445-456.
87. Tyzack GE, Sitnikov S, Barson D, et al. Astrocyte response to motor neuron injury promotes structural synaptic plasticity via STAT3-regulated TSP-1 expression. Nat Commun 2014; 5:4294.
88. Fiandaca MS, Kapogiannis D, Mapstone M, et al. Identification of preclinical Alzheimer's disease by a profile of pathogenic proteins in neurally derived blood exosomes: a case-control study. Alzheimers Dement 2015; 11:600-607.
89. Stocchetti N, Taccone FS, Citerio G, et al. Neuroprotection in acute brain injury: an up-to-date review. Crit Care 2015; 19:186.
90. Mellott TJ, Pender SM, Burke RM, et al. IGF2 ameliorates amyloidosis, increases cholinergic marker expression and raises BMP9 and neurotrophin levels in the hippocampus of the APPswePS1dE9 Alzheimer's disease model mice. PLoS One 2014; 9:e94287.
91. Xin H, Li Y, Buller B, et al. Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells 2012; 30:1556-1564.
92. Maumus M, Jorgensen C, Noel D. Mesenchymal stem cells in regenerative medicine applied to rheumatic diseases: role of secretome and exosomes. Biochimie 2013; 95:2229-2234.
93. Takeda YS, Xu Q. Neuronal differentiation of human mesenchymal stem cells using exosomes derived from differentiating neuronal cells. PLoS One 2015; 10:e0135111.
94. Bahrini I, Song JH, Diez D, Hanayama R. Neuronal exosomes facilitate synaptic pruning by up-regulating complement factors in microglia. Sci Rep 2015; 5:7989.
95. Zhuang X, Xiang X, Grizzle W, et al. Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol Ther 2011; 19:1769-1779.