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International Journal of Alzheimer’s Disease
Volume 2012, Article ID 608732, 5 pages
http://dx.doi.org/10.1155/2012/608732
Review Article

Traumatic Brain Injury, Microglia, and Beta Amyloid

1Division of Emergency Medicine, Department of Medicine, Children’s Hospital Boston, Harvard Medical School, Boston, MA 02124, USA
2Neuroscience Center, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02129, USA
3Department of Pediatrics, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02129, USA

Received 30 November 2011; Accepted 2 March 2012

Academic Editor: Joseph El Khoury

Copyright © 2012 Rebekah C. Mannix and Michael J. Whalen. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V. E. Johnson, W. Stewart, and D. H. Smith, “Traumatic brain injury and amyloid-β pathology: a link to Alzheimer's disease?” Nature Reviews Neuroscience, vol. 11, no. 5, pp. 361–370, 2010. View at Google Scholar · View at Scopus
  2. V. E. Johnson, W. Stewart, D. I. Graham, J. E. Stewart, A. H. Praestgaard, and D. H. Smith, “A neprilysin polymorphism and amyloid-β plaques after traumatic brain injury,” Journal of Neurotrauma, vol. 26, no. 8, pp. 1197–1202, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. J. A. Mortimer, L. R. French, J. T. Hutton, and L. M. Schuman, “Head injury as a risk factor for Alzheimer's disease,” Neurology, vol. 35, no. 2, pp. 264–267, 1985. View at Google Scholar · View at Scopus
  4. A. B. Graves, E. White, T. D. Koepsell et al., “The association between head trauma and Alzheimer's disease,” American Journal of Epidemiology, vol. 131, no. 3, pp. 491–501, 1990. View at Google Scholar · View at Scopus
  5. J. A. Mortimer, C. M. van Duijn, V. Chandra et al., “Head trauma as a risk factor for Alzheimer's disease: a collaborative re-analysis of case-control studies. EURODEM Risk Factors Research Group,” International Journal of Epidemiology, vol. 20, supplement 2, pp. S28–S35, 1991. View at Google Scholar
  6. E. Salib and V. Hillier, “Head injury and the risk of Alzheimer's disease: a case control study,” International Journal of Geriatric Psychiatry, vol. 12, pp. 363–368, 1997. View at Google Scholar
  7. Z. Guo, L. A. Cupples, A. Kurz et al., “Head injury and the risk of AD in the MIRAGE study,” Neurology, vol. 54, no. 6, pp. 1316–1323, 2000. View at Google Scholar · View at Scopus
  8. G. W. Roberts, S. M. Gentleman, A. Lynch, and D. I. Graham, “βA4 amyloid protein deposition in brain after head trauma,” The Lancet, vol. 338, no. 8780, pp. 1422–1423, 1991. View at Publisher · View at Google Scholar · View at Scopus
  9. G. W. Roberts, S. M. Gentleman, A. Lynch, L. Murray, M. Landon, and D. I. Graham, “β amyloid protein deposition in the brain after severe head injury: implications for the pathogenesis of Alzheimer's disease,” Journal of Neurology Neurosurgery and Psychiatry, vol. 57, no. 4, pp. 419–425, 1994. View at Google Scholar · View at Scopus
  10. M. T. Giordana, A. Attanasio, P. Cavalla, A. Migheli, M. C. Vigliani, and D. Schiffer, “Reactive cell proliferation and microglia following injury to the rat brain,” Neuropathology and Applied Neurobiology, vol. 20, no. 2, pp. 163–174, 1994. View at Google Scholar · View at Scopus
  11. W. J. Streit, “The role of microglia in brain injury,” NeuroToxicology, vol. 17, no. 3-4, pp. 671–678, 1996. View at Google Scholar · View at Scopus
  12. S. E. Hickman, E. K. Allison, and J. El Khoury, “Microglial dysfunction and defective β-amyloid clearance pathways in aging alzheimer's disease mice,” The Journal of Neuroscience, vol. 28, no. 33, pp. 8354–8360, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Mandrekar, Q. Jiang, C. Y. D. Lee, J. Koenigsknecht-Talboo, D. M. Holtzman, and G. E. Landreth, “Microglia mediate the clearance of soluble aβ through fluid phase macropinocytosis,” The Journal of Neuroscience, vol. 29, no. 13, pp. 4252–4262, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. J. C. M. Schlachetzki and M. Hüll, “Microglial activation in Alzheimer's disease,” Current Alzheimer Research, vol. 6, no. 6, pp. 554–563, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Engel, H. Schluesener, M. Mittelbronn et al., “Dynamics of microglial activation after human traumatic brain injury are revealed by delayed expression of macrophage-related proteins MRP8 and MRP14,” Acta Neuropathologica, vol. 100, no. 3, pp. 313–322, 2000. View at Google Scholar · View at Scopus
  16. S. M. Gentleman, P. D. Leclercq, L. Moyes et al., “Long-term intracerebral inflammatory response after traumatic brain injury,” Forensic Science International, vol. 146, no. 2-3, pp. 97–104, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. T. K. McIntosh, K. E. Saatmann, R. Raghupathi et al., “The Dorothy Russell memorial lecture. The molecular and cellular sequelae of experimental traumatic brain injury: pathogenetic mechanisms,” Neuropathology and Applied Neurobiology, vol. 24, no. 4, pp. 251–267, 1998. View at Publisher · View at Google Scholar · View at Scopus
  18. D. Davalos, J. Grutzendler, G. Yang et al., “ATP mediates rapid microglial response to local brain injury in vivo,” Nature Neuroscience, vol. 8, no. 6, pp. 752–758, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. R. Beschorner, T. D. Nguyen, F. Gözalan et al., “CD14 expression by activated parenchymal microglia/macrophages and infiltrating monocytes following human traumatic brain injury,” Acta Neuropathologica, vol. 103, no. 6, pp. 541–549, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. A. F. Ramlackhansingh, D. J. Brooks, R. J. Greenwood et al., “Inflammation after trauma: microglial activation and traumatic brain injury,” Annals of Neurology, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Csuka, V. H. J. Hans, E. Ammann, O. Trentz, T. Kossmann, and M. C. Morganti-Kossmann, “Cell activation and inflammatory response following traumatic axonal injury in the rat,” NeuroReport, vol. 11, no. 11, pp. 2587–2590, 2000. View at Google Scholar · View at Scopus
  22. J. Maeda, M. Higuchi, M. Inaji et al., “Phase-dependent roles of reactive microglia and astrocytes in nervous system injury as delineated by imaging of peripheral benzodiazepine receptor,” Brain Research, vol. 1157, no. 1, pp. 100–111, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Gehrmann, “Microglia: a sensor to threats in the nervous system?” Research in Virology, vol. 147, no. 2-3, pp. 79–88, 1996. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Koshinaga, Y. Katayama, M. Fukushima, H. Oshima, T. Suma, and T. Takahata, “Rapid and widespread microglial activation induced by traumatic brain injury in rat brain slices,” Journal of Neurotrauma, vol. 17, no. 3, pp. 183–192, 2000. View at Google Scholar · View at Scopus
  25. C. Israelsson, H. Bengtsson, A. Kylberg et al., “Distinct cellular patterns of upregulated chemokine expression supporting a prominent inflammatory role in traumatic brain injury,” Journal of Neurotrauma, vol. 25, no. 8, pp. 959–974, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. J. F. Stover, B. Schöning, T. F. Beyer, C. Woiciechowsky, and A. W. Unterberg, “Temporal profile of cerebrospinal fluid glutamate, interleukin-6, and tumor necrosis factor-α in relation to brain edema and contusion following controlled cortical impact injury in rats,” Neuroscience Letters, vol. 288, no. 1, pp. 25–28, 2000. View at Publisher · View at Google Scholar · View at Scopus
  27. K. T. Lu, Y. W. Wang, J. T. Yang, Y. L. Yang, and H. I. Chen, “Effect of interleukin-1 on traumatic brain injury-induced damage to hippocampal neurons,” Journal of Neurotrauma, vol. 22, no. 8, pp. 885–895, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. E. Pinteaux, L. C. Parker, N. J. Rothwell, and G. N. Luheshi, “Expression of interleukin-1 receptors and their role in interleukin-1 actions in murine microglial cells,” Journal of Neurochemistry, vol. 83, no. 4, pp. 754–763, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. N. Rothwell, “Interleukin-1 and neuronal injury: mechanisms, modification, and therapeutic potential,” Brain, Behavior, and Immunity, vol. 17, no. 3, pp. 152–157, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. E. Csuka, M. C. Morganti-Kossmann, P. M. Lenzlinger, H. Joller, O. Trentz, and T. Kossmann, “IL-10 levels in cerebrospinal fluid and serum of patients with severe traumatic brain injury: relationship to IL-6, TNF-α, TGF-β1 and blood-brain barrier function,” Journal of Neuroimmunology, vol. 101, no. 2, pp. 211–221, 1999. View at Publisher · View at Google Scholar · View at Scopus
  31. S. M. Knoblach and A. I. Faden, “Interleukin-10 improves outcome and alters proinflammatory cytokine expression after experimental traumatic brain injury,” Experimental Neurology, vol. 153, no. 1, pp. 143–151, 1998. View at Publisher · View at Google Scholar · View at Scopus
  32. S. G. Kremlev and C. Palmer, “Interleukin-10 inhibits endotoxin-induced pro-inflammatory cytokines in microglial cell cultures,” Journal of Neuroimmunology, vol. 162, no. 1-2, pp. 71–80, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. Hamada, T. Ikata, S. Katoh et al., “Effects of exogenous transforming growth factor-β1 on spinal cord injury in rats,” Neuroscience Letters, vol. 203, no. 2, pp. 97–100, 1996. View at Publisher · View at Google Scholar · View at Scopus
  34. W. R. Tyor, N. Avgeropoulos, G. Ohlandt, and E. L. Hogan, “Treatment of spinal cord impact injury in the rat with transforming growth factor-β,” Journal of the Neurological Sciences, vol. 200, no. 1-2, pp. 33–41, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Rogers and L. F. Lue, “Microglial chemotaxis, activation, and phagocytosis of amyloid β-peptide as linked phenomena in Alzheimer's disease,” Neurochemistry International, vol. 39, no. 5-6, pp. 333–340, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. M. D. Ikonomovic, K. Uryu, E. E. Abrahamson et al., “Alzheimer's pathology in human temporal cortex surgically excised after severe brain injury,” Experimental Neurology, vol. 190, no. 1, pp. 192–203, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Iwata, X. H. Chen, T. K. McIntosh, K. D. Browne, and D. H. Smith, “Long-term accumulation of amyloid-β in axons following brain trauma without persistent upregulation of amyloid precursor protein genes,” Journal of Neuropathology and Experimental Neurology, vol. 61, no. 12, pp. 1056–1068, 2002. View at Google Scholar · View at Scopus
  38. K. Uryu, H. Laurer, T. McIntosh et al., “Repetitive mild brain trauma accelerates Abeta deposition, lipid peroxidation, and cognitive impairment in a transgenic mouse model of Alzheimer amyloidosis,” The Journal of Neuroscience, vol. 22, pp. 446–454, 2002. View at Google Scholar
  39. D. J. Loane, A. Pocivavsek, C. E. H. Moussa et al., “Amyloid precursor protein secretases as therapeutic targets for traumatic brain injury,” Nature Medicine, vol. 15, no. 4, pp. 377–379, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. R. C. Mannix, J. Zhang, J. Park et al., “Age-dependent effect of apolipoprotein E4 on functional outcome after controlled cortical impact in mice,” Journal of Cerebral Blood Flow and Metabolism, vol. 31, no. 1, pp. 351–361, 2011. View at Google Scholar
  41. I. Blasko, R. Beer, M. Bigl et al., “Experimental traumatic brain injury in rats stimulates the expression, production and activity of Alzheimer's disease β-secretase (BACE-1),” Journal of Neural Transmission, vol. 111, no. 4, pp. 523–536, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. X. H. Chen, R. Siman, A. Iwata, D. F. Meaney, J. Q. Trojanowski, and D. H. Smith, “Long-term accumulation of amyloid-β, β-secretase, presenilin-1, and caspase-3 in damaged axons following brain trauma,” American Journal of Pathology, vol. 165, no. 2, pp. 357–371, 2004. View at Google Scholar · View at Scopus
  43. Y. Nadler, A. Alexandrovich, N. Grigoriadis et al., “Increased expression of the γ-secretase components presenilin-1 and nicastrin in activated astrocytes and microglia following traumatic brain injury,” GLIA, vol. 56, no. 5, pp. 552–567, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. Y. F. Liaoi, B. J. Wang, H. T. Cheng, L. H. Kuo, and M. S. Wolfe, “Tumor necrosis factor-α, interleukin-1β, and interferon-γ stimulate γ-secretase-mediated cleavage of amyloid precursor protein through a JNK-dependent MAPK pathway,” Journal of Biological Chemistry, vol. 279, no. 47, pp. 49523–49532, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. W. S. T. Griffin, J. G. Sheng, S. M. Gentleman, D. I. Graham, R. E. Mrak, and G. W. Roberts, “Microglial interleukin-1α expression in human head injury: correlations with neuronal and neuritic P-amyloid precursor protein expression,” Neuroscience Letters, vol. 176, no. 2, pp. 133–136, 1994. View at Publisher · View at Google Scholar · View at Scopus
  46. X. H. Chen, V. E. Johnson, K. Uryu, J. Q. Trojanowski, and D. H. Smith, “A lack of amyloid β plaques despite persistent accumulation of amyloid β in axons of long-term survivors of traumatic brain injury,” Brain Pathology, vol. 19, no. 2, pp. 214–223, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. R. O. Sanchez Mejia, V. O. Ona, M. Li, and R. M. Friedlander, “Minocycline reduces traumatic brain injury-mediated caspase-1 activation, tissue damage, and neurological dysfunction,” Neurosurgery, vol. 48, no. 6, pp. 1393–1401, 2001. View at Google Scholar · View at Scopus
  48. N. Bye, M. D. Habgood, J. K. Callaway et al., “Transient neuroprotection by minocycline following traumatic brain injury is associated with attenuated microglial activation but no changes in cell apoptosis or neutrophil infiltration,” Experimental Neurology, vol. 204, no. 1, pp. 220–233, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. E. Siopi, A. H. Cho, S. Homsi et al., “Minocycline restores sAPPalpha levels and reduces the late histopathological consequences of traumatic brain injury in mice,” Journal of Neurotrauma, vol. 28, pp. 2135–2143, 2011. View at Google Scholar
  50. A. B. Jaffe, C. D. Toran-Allerand, P. Greengard, and S. E. Gandy, “Estrogen regulates metabolism of Alzheimer amyloid β precursor protein,” The Journal of Biological Chemistry, vol. 269, no. 18, pp. 13065–13068, 1994. View at Google Scholar · View at Scopus
  51. E. Kojro, G. Gimpl, S. Lammich, W. März, and F. Fahrenholz, “Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the α-secretase ADAM 10,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 10, pp. 5815–5820, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. B. S. Kasturi and D. G. Stein, “Progesterone decreases cortical and sub-cortical edema in young and aged ovariectomized rats with brain injury,” Restorative Neurology and Neuroscience, vol. 27, no. 4, pp. 265–275, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. B. Li, A. Mahmood, D. Lu et al., “Simvastatin attenuates microglial cells and astrocyte activation and decreases interleukin-1B level after traumatic brain injury,” Neurosurgery, vol. 65, no. 1, pp. 179–185, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. H. Wang, L. Durham, H. Dawson et al., “An apolipoprotein E-based therapeutic improves outcome and reduces Alzheimer's disease pathology following closed head injury: evidence of pharmacogenomic interaction,” Neuroscience, vol. 144, no. 4, pp. 1324–1333, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. E. E. Abrahamson, M. D. Ikonomovic, C. Edward Dixon, and S. T. DeKosky, “Simvastatin therapy prevents brain trauma-induced increases in β-amyloid peptide levels,” Annals of Neurology, vol. 66, no. 3, pp. 407–414, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. D. J. Loane, P. M. Washington, L. Vardanian et al., “Modulation of ABCA1 by an LXR agonist reduces beta-amyloid levels and improves outcome after traumatic brain injury,” Journal of Neurotrauma, vol. 28, no. 2, pp. 225–236, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. P. E. Cramer, J. R. Cirrito, D. W. Wesson et al., “ApoE-directed therapeutics rapidly clear beta-amyloid and reverse deficits in AD mouse models,” Science, vol. 335, no. 6075, pp. 1503–1506, 2012. View at Google Scholar