Glial cell-mediated deterioration and repair of the nervous system after traumatic brain injury in a rat model as assessed by positron emission tomography

Journal of Neurotrauma

Volumn 27, Issue 8, 2010, Pages 1463-1475

  Yu, Iwae ^a,b   Inaji, Motoki ^a,b   Maeda, Jun ^a   Okauchi, Takashi ^a   Nariai, Tadashi ^b   Ohno, Kikuo ^b   Higuchi, Makoto ^a   Suhara, Tetsuya ^a  

^a NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

glial cell response to injury; head trauma; inflammation; models of injury; positron emission tomography scanning

Indexed keywords

FLUORODEOXYGLUCOSE F 18; FLUOROETHYL DAA1106 F 18; TRACER; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTORADIOGRAPHY; FRONTAL CORTEX; GLIA CELL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MACROPHAGE; MALE; MICROGLIA; NERVE CELL LESION; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; RAT; TRAUMATIC BRAIN INJURY;

ANIMALS; AUTORADIOGRAPHY; BRAIN HEMORRHAGE, TRAUMATIC; FLUORODEOXYGLUCOSE F18; GLIOSIS; IMMUNOHISTOCHEMISTRY; MALE; MITOCHONDRIAL ADP, ATP TRANSLOCASES; NERVE REGENERATION; NEUROGLIA; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; RATS; RATS, WISTAR;

EID: 77955888790     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2009.1196     Document Type: Article

References (47)

1. Alavi, A. (1989). Functional and anatomical studies of head injury. J. Neuropsychiatry Clin. Neurosci. 1, S45-S50.
2. Bergsneider, M., Hovda, D.A., Lee, S.M., Kelly, D.F., McArthur, D.L., Vespa, P.M., Lee, J.H., Huang, S.C., Martin, N.A., Phelps, M.E., and Becker, D.P. (2000). Dissociation of cerebral glucose metabolism and level of consciousness during the period of metabolic depression following human traumatic brain injury. J. Neurotrauma 17, 389-401.
3. Bergsneider, M., Hovda, D.A., McArthur, D.L., Etchepare, M, Huang, S.C., Sehati, N., Satz, P., Phelps, M.E., and Becker, D.P. (2001). Metabolic recovery following human traumatic brain injury based on FDG-PET: time course and relationship to neurological disability. J. Head Trauma Rehabil 16, 135-148.
4. Browne, K.D., Iwata, A., Putt, M.E., and Smith, D.H. (2006) Chronic ibuprofen administration worsens cognitive outcome following traumatic brain injury in rats. Exp. Neurol. 201, 301-307.
5. Cagnin, A., Brooks, D.J., Kennedy, A.M., Gunn, R.N., Myers, R., Turkheimer, F.E., Jones, T., and Banati, R.B. (2001). In-vivo measurement of activated microglia in dementia. Lancet 358, 461-467.
6. Cavus, I., Kasoff, W.S., Cassaday, M.P., Jacob, R., Gueorguieva, R., Sherwin, R.S., Krystal, J.H., Spencer, D.D., and Abi-Saab, W.M. (2005). Extracellular metabolites in the cortex and hippocampus of epileptic patients. Ann. Neurol. 57, 226-235.
7. Cernak, I., O'Connor, C., and Vink, R. (2002) Inhibition of cyclooxygenase 2 by nimesulide improves cognitive outcome more than motor outcome following diffuse traumatic brain injury in rats. Exp. Brain Res. 147, 193-199.
8. Chen, M.K., Baidoo, K., Verina, T., and Guilarte, T.R. (2004). Peripheral benzodiazepine receptor imaging in CNS demyelination: functional implications of anatomical and cellular localization. Brain 127, 1379-1392.
9. Cicchetti, F., Brownell, A.L., Williams, K., Chen, Y.I., Livni, E., and Isacson, O. (2002). Neuroinflammation of the nigrostriatal pathway during progressive 6-OHDA dopamine degeneration in rats monitored by immunohistochemistry and PET imaging. Eur. J. Neurosci. 15, 991-998.
10. Dietrich, W.D., Alonso, O., Busto, R., and Ginsberg, M.D. (1994). Widespread metabolic depression and reduced somatosensory circuit activation following traumatic brain injury in rats. J. Neurotrauma 11, 629-640.
11. Dixon, C.E., Lyeth, B.G., Povlishock, J.T., Findling, R.L., Hamm, R.J., Marmarou, A., and Young, H.F. (1987). A fluid percussion model of experimental brain injury in the rat. J. Neurosurg. 67, 110-119.
12. Homsi, S., Piaggio, T., Croci, N., Noble, F., Plotkine, M., Marchand-Leroux, C., and Jafarian-Tehrani, M. (2010) Blockade of acute microglial activation by minocycline promotes neuroprotection and reduces locomotor hyperactivity following closed head injury in mice: a twelve-week follow-up study. J. Neurotrauma 27, 911-921.
13. Humayun, M.S., Presty, S.K., Lafrance, N.D., Holcomb, H.H., Loats, H., Long, D.M., Wagner, H.N., and Gordon, B. (1989). Local cerebral glucose abnormalities in mild closed head injured patients with cognitive impairments. Nucl. Med. Commun. 10, 335-344.
14. Ip, E.Y., Zanier, E.R., Moore, A.H., Lee, S.M., and Hovda, D.A. (2003). Metabolic, neurochemical, and histologic responses to vibrissa motor cortex stimulation after traumatic brain injury. J. Cereb. Blood Flow Metab. 23, 300-910.
15. Ji, B., Maeda, J., Sawada, M., Ono, M., Okauchi, T., Inaji, M., Zhang, M.R., Suzuki, K., Ando, K., Staufenbiel, M., Trojanowski, J.Q., Lee, V.M., Higuchi, M., and Suhara, T. (2008). Imaging of peripheral benzodiazepine receptor expression as biomarkers of detrimental versus beneficial glial responses in mouse models of Alzheimer's and other CNS pathologies. J. Neurosci. 28, 12255-12267.
16. Laird, M.D., Vender, J.R., and Dhandapani, K.M. (2008). Opposing roles for reactive astrocytes following traumatic brain injury. Neurosignals 16, 154-164.
17. Langfitt, T.W., Obrist, W.D., Alavi, A., Grossman, R.I., Zimmerman, R., Jaggi, J., Uzzell, B., Reivich, M., and Patton, D.R. (1986). Computerized tomography, magnetic resonance imaging, and positron emission tomography in the study of brain trauma. Preliminary observations. J. Neurosurg. 64, 760-767.
18. Lloyd, E., Somera-Molina, K., Van, Eldik, L.J., Watterson, D.M., and Wainwright, M.S. (2008). Suppression of acute proinflammatory cytokine and chemokine upregulation by post-injury administration of a novel small molecule improves long-term neurologic outcome in a mouse model of traumatic brain injury. J. Neuroinflammation 5, 28
19. Mac Donald, C.L., Dikranian, K., Bayly, P., Holtzman, D., and Brody, D. (2007). Diffusion tensor imaging reliably detects experimental traumatic axonal injury and indicates approximate time of injury. J. Neurosci. 27, 11869-11876.
20. Maeda, J., Higuchi, M., Inaji, M., Ji, B., Haneda, E., Okauchi, T., Zhang, M.R., Suzuki, K., and Suhara, T. (2007a). Phasedependent roles of reactive microglia and astrocytes in nervous system injury as delineated by imaging of peripheral benzodiazepine receptor. Brain Res. 1157, 100-111.
21. Maeda, J., Ji, B., Irie, T., Tomiyama, T., Maruyama, M., Okauchi, T., Staufenbiel, M., Iwata, N., Ono, M., Saido, T.C., Suzuki, K., Mori, H., Higuchi, M., and Suhara, T. (2007b). Longitudinal, quantitative assessment of amyloid, neuroinflammation, and anti-amyloid treatment in a living mouse model of Alzheimer's disease enabled by positron emission tomography. J. Neurosci. 27, 10957-10968.
22. Maeda, J., Suhara, T., Zhang, M.R., Okauchi, T., Yasuno, F., Ikoma, Y., Inaji, M., Nagai, Y., Takano, A., Obayashi, S., and Suzuki, K. (2004). Novel peripheral benzodiazepine receptor ligand [11C]DAA1106 for PET: an imaging tool for glial cells in the brain. Synapse 52, 283-291.
23. Magistretti, P.J., and Pellerin, L. (1999). Astrocytes couple synaptic activity to glucose utilization in the brain. News Physiol. Sci. 14, 177-182.
24. Magistretti, P.J., Pellerin, L., Rothman, D.L., and Shulman, R.G. (1999). Energy on demand. Science 283, 496-497.
25. McIntosh, T.K., Vink, R., Noble, L., Yamakami, I., Fernyak, S., Soares, H., and Faden, A.I. (1989). Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28, 233-244. (Pubitemid 19026758)
26. Moore, A.H., Osteen, C.L., Chatziioannou, A.F., Hovda, D.A., and Cherry, S.R. (2000). Quantitative assessment of longitudinal metabolic changes in vivo after traumatic brain injury in the adult rat using FDG-microPET. J. Cereb. Blood Flow Metab. 20, 1492-1501.
27. Morganti-Kossmann, M.C., Satgunaseelan, L., Bye, N., and Kossmann, T. (2007). Modulation of immune response by head injury. Injury 38, 1392-1400.
28. Myers, R., Manjil, L.G., Cullen, B.M., Price, G.W., Frackowiak, R.S., and Cremer, J.E. (1991). Macrophage and astrocyte populations in relation to [3H]PK 11195 binding in rat cerebral cortex following a local ischaemic lesion. J. Cereb. Blood Flow Metab. 11, 314-322.
29. Ouchi, Y., Yoshikawa, E., Sekine, Y., Futatsubashi, M., Kanno, T., Ogusu, T., and Torizuka, T. (2005). Microglial activation and dopamine terminal loss in early Parkinson's disease. Ann. Neurol. 57, 168-175.
30. Raghavendra Rao, V.L., Dogan, A., Bowen, K.K., and Dempsey, R.J. (2000). Traumatic brain injury leads to increased expression of peripheral-type benzodiazepine receptors, neuronal death, and activation of astrocytes and microglia in rat thalamus. Exp. Neurol. 161, 102-114.
31. Richards, D.A., Tolias, C.M., Sgouros, S., and Bowery, N.G. (2003). Extracellular glutamine to glutamate ratio may predict outcome in the injured brain: a clinical microdialysis study in children. Pharmacol. Res. 48, 101-109.
32. Rojas, S., Martin, A., Arranz, M.J., Pareto, D., Purroy, J., Verdaguer, E., Llop, J., Gomez, V., Gispert, J.D.,Millan, O., Chamorro, A., and Planas, A.M. (2007). Imaging brain inflammation with [(11)C]PK11195 by PET and induction of the peripheral-type benzodiazepine receptor after transient focal ischemia in rats. J. Cereb. Blood Flow Metab. 27, 1975-1986.
33. Sanchez Mejia, R.O., Ona, V.O., Li, M., and Friedlander, R.M. (2001) Minocycline reduces traumatic brain injury-mediated caspase-1 activation, tissue damage, and neurological dysfunction. Neurosurgery 48, 1393-1399.
34. Shen, J., Petersen, K.F., Behar, K.L., Brown, P., Nixon, T.W., Mason, G.F., Petroff, O.A., Shulman, G.I., Shulman, R.G., and Rothman, D.L. (1999). Determination of the rate of the glutamate/ glutamine cycle in the human brain by in vivo 13C NMR. Proc. Natl. Acad. Sci. USA 96, 8235-8240.
35. Shimoji, K., Ravasi, L., Schmidt, K., Soto-Montenegro, M.L., Esaki, T., Seidel, J., Jagoda, E., Sokoloff, L., Green, M.V., and Eckelman, W.C. (2004). Measurement of cerebral glucose metabolic rates in the anesthetized rat by dynamic scanning with 18F-FDG, the ATLAS small animal PET scanner, and arterial blood sampling. J. Nucl. Med. 45, 665-672.
36. Smith, D.H., Meaney, D.F., and Shull, W.H. (2003). Diffuse axonal injury in head trauma. J. Head Trauma Rehabil. 18, 307-316.
37. Stephenson, D.T., Schober, D.A., Smalstig, E.B., Mincy, R.E., Gehlert, D.R., and Clemens, J.A. (1995). Peripheral benzodiazepine receptors are colocalized with activated microglia following transient global forebrain ischemia in the rat. J. Neurosci. 15, 5263-5274.
38. Tai, Y.C., Ruangma, A., Rowland, D., Siegel, S., Newport, D.F., Chow, P.L., and Laforest, R. (2005). Performance evaluation of the microPET focus: a third-generation microPET scanner dedicated to animal imaging. J. Nucl. Med. 46, 455-463.
39. Thompson, H.J., Lifshitz, J., Marklund, N., Grady, M.S., Graham, D.I., Hovda, D.A., and McIntosh, T.K. (2005). Lateral fluid percussion brain injury: a 15-year review and evaluation. J. Neurotrauma 22, 42-75.
40. Toyama, H., Ichise, M., Liow, J.S., Modell, K.J., Vines, D.C., Esaki, T., Cook, M., Seidel, J., Sokoloff, L., Green, M.V., and Innis, R.B. (2004). Absolute quantification of regional cerebral glucose utilization in mice by 18F-FDG small animal PET scanning and 2-14C-DG autoradiography. J. Nucl. Med. 45, 1398-1405.
41. Venneti, S., Lopresti, B.J., Wang, G., Hamilton, R.L., Mathis, C.A., Klunk, W.E., Apte, U.M., and Wiley, C.A. (2009). PK11195 labels activated microglia in Alzheimer's disease and in vivo in a mouse model using PET. Neurobiol. Aging 30, 1217-1226.
42. Venneti, S., Lopresti, B.J., Wang, G., Slagel, S.L., Mason, N.S., Mathis, C.A., Fischer, M.L., Larsen, N.J., Mortimer, A.D., Hastings, T.G., Smith, A.D., Zigmond, M.J., Suhara, T., Higuchi, M., and Wiley, C.A. (2007). A comparison of the highaffinity peripheral benzodiazepine receptor ligands DAA1106 and (R)-PK11195 in rat models of neuroinflammation: implications for PET imaging of microglial activation. J. Neurochem. 102, 2118-2131.
43. Wegman, T.D., Maas, B., Elsinga, P.H., and Vaalburg, W. (2002). An improved method for the preparation of [11C]verapamil. Appl. Radiat. Isot. 57, 505-507.
44. Yamaki, T., Yoshino, E., Fujimoto, M., Ohmori, Y., Imahori, Y., and Ueda, S. (1996). Chronological positron emission tomographic study of severe diffuse traumatic brain injury in the chronic stage. J. Trauma 40, 50-56.
45. Yasuno, F., Ota, M., Kosaka, J., Ito, H., Higuchi, M., Doronbekov, T.K., Nozaki, S., Fujimura, Y., Koeda, M., Asada, T., and Suhara, T. (2008). Increased binding of peripheral benzodiazepine receptor in Alzheimer's disease measured by positron emission tomography with [11C]DAA1106. Biol. Psychiatry 64, 835-841.
46. Yoshiyama, Y., Higuchi, M., Zhang, B., Huang, S.M., Iwata, N., Saido, T.C., Maeda, J., Suhara, T., Trojanowski, J.Q., and Lee, V.M. (2007). Synapse loss and microglial activation precede tangles in a P301S tauopathy mousemodel.Neuron 53, 337-351.
47. Zhang, M.R., Maeda, J., Ogawa, M., Noguchi, J., Ito, T., Yoshida, Y., Okauchi, T., Obayashi, S., Suhara, T., and Suzuki, K. (2004). Development of a new radioligand, N-(5-fluoro-2-phenoxyphenyl)-N-(2-[18F]fluoroethyl-5- methoxybenzyl) acetamide, for PET imaging of peripheral benzodiazepine receptor in primate brain. J. Med. Chem. 47, 2228-2235.