Preventing flow-metabolism uncoupling acutely reduces axonal injury after traumatic brain injury

Journal of Neurotrauma

Volumn 29, Issue 7, 2012, Pages 1469-1482

  Harris, Neil G ^a   Mironova, Yevgeniya A ^a   Chen, Szu Fu ^b,c   Richards, Hugh K ^d,e   Pickard, John D ^d,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CHENG HSIN GENERAL HOSPITAL   (Taiwan)

^c NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

autoradiography; blood flow; cortical contusion injury; glucose metabolism; uncoupling

Indexed keywords

ACETAZOLAMIDE; FLUORODEOXYGLUCOSE F 18; IODOPHENAZONE C 14;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; AXOPLASM FLOW; BRAIN BLOOD FLOW; BRAIN METABOLISM; CLINICAL ASSESSMENT; CONTROLLED STUDY; CORPUS CALLOSUM; CORTICAL AMYGDALA; DATA ANALYSIS; DISEASE SEVERITY; HYPOTHESIS; MEDICAL RECORD; NEUROFILAMENT; NONHUMAN; RAT; STAINING; STEREOMETRY; TRAUMATIC BRAIN INJURY;

ACETAZOLAMIDE; ANIMALS; BRAIN INJURIES; CEREBROVASCULAR CIRCULATION; DIFFUSE AXONAL INJURY; ENERGY METABOLISM; MALE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84860273214     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.2161     Document Type: Article

References (69)

1. Adams, J.H., Doyle, D., Ford, I., Gennarelli, T.A, Graham, D.I, and McLellan, D.R. (1989). Diffuse axonal injury in head injury: Definition, diagnosis and grading. Histopathology 15, 49-59.
2. Belayev, L., Alonso, O.F., Huh, P.W, Zhao, W., Busto, R., and Ginsberg, M.D. (1999). Post treatment with high-dose albumin reduces histopathological damage and improves neurologicaldeficit following fluid percussion brain injury in rats. J. Neurotrauma 16, 445-453.
3. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Statist. Soc. 57, 289-300.
4. Bergsneider, M., Hovda, D.A., Shalmon, E., Kelly, D.F., Vespa, P.M., Martin, N.A., Phelps, M.E., McArthur, D.L., Caron, M.J., Kraus, J.F., and Becker, D.P. (1997). Cerebral hyperglycolysis following severe traumatic brain injury in humans: A positron emission tomography study. J. Neurosurg. 86, 241-251.
5. Bickler, P.E., Litt, L., Banville, D.L., and Severinghaus, J.W. (1988). Effects of acetazolamide on cerebral acid-base balance. J. Appl. Physiol. 65, 422-427.
6. Bouma, G.J., and Muizelaar, J.P. (1992). Cerebral blood flow, cerebral blood volume, and cerebrovascular reactivity after severe head injury. J. Neurotrauma 9(Suppl. 1), S333-S348.
7. Bouma, G.J., Muizelaar, J.P., Choi, S.C., Newlon, P.G., and Young, H.F. (1991). Cerebral circulation and metabolism after severe traumatic brain injury: The elusive role of ischemia. J. Neurosurg. 75, 685-693.
8. Bramlett, H.M., Green, E.J., Dietrich, W.D., Busto, R., Globus, M.Y., and Ginsberg, M.D. (1995). Posttraumatic brain hypothermia provides protection from sensorimotor and cognitive behavioral deficits. J. Neurotrauma 12, 289-298.
9. Bryan, R.M., Jr., Cherian, L., and Robertson, C. (1995). Regional cerebral blood flow after controlled cortical impact injury in rats. Anesth. Analg. 80, 687-695.
10. Buki, A., Okonkwo, D.O., and Povlishock, J.T. (1999a). Postinjury cyclosporin A administration limits axonal damage and disconnection in traumatic brain injury. J. Neurotrauma 16, 511-521.
11. Buki, A., Okonkwo, D.O., Wang, K.K., and Povlishock, J.T. (2000). Cytochrome c release and caspase activation in traumatic axonal injury. J. Neurosci. 20, 2825-2834.
12. Buki, A., Siman, R., Trojanowski, J.Q., and Povlishock, J.T. (1999b). The role of calpain-mediated spectrin proteolysis in traumatically induced axonal injury. J. Neuropathol. Exp. Neurol. 58, 365-375.
13. Chen, S., Pickard, J.D., and Harris, N.G. (2003). Time-course of cellular pathology after controlled cortical impact injury. Exp. Neurol. 182, 87-102.
14. Chen, S., Richards, H.K., Smielewski, P., Johnstrom, P., Salvador, R., Pickard, J.D., and Harris, N.G. (2004). Relationship between flow-metabolism uncoupling and evolving axonal injury after experimental traumatic brain injury. J. Cereb. Blood Flow Metab. 24, 1025-1036.
15. Chen, T., Qian, Y.Z., Rice, A., Zhu, J.P., Di, X., and Bullock, R. (2000). Brain lactate uptake increases at the site of impact after traumatic brain injury. Brain Res. 861, 281-287.
16. Cherian, L., Chacko, G., Goodman, J.C., and Robertson, C.S. (1999). Cerebral hemodynamic effects of phenylephrine and Larginine after cortical impact injury. Crit. Care Med. 27, 2512-2517.
17. Christman, C.W., Grady, M.S., Walker, S.A., Holloway, K.L., and Povlishock, J.T. (1994). Ultrastructural studies of diffuse axonal injury in humans. J. Neurotrauma 11, 173-186.
18. Coles, J.P., Minhas, P.S., Fryer, T.D., Smielewski, P., Aigbirihio, F., Donovan, T., Downey, S.P., Williams, G., Chatfield, D., Matthews, J.C., Gupta, A.K., Carpenter, T.A., Clark, J.C., Pickard, J.D., and Menon, D.K. (2002). Effect of hyperventilation on cerebral blood flow in traumatic head injury: Clinical relevance and monitoring correlates. Crit. Care Med. 30, 1950-1959.
19. Forbes, M.L., Hendrich, K.S., Kochanek, P.M., Williams, D.S., Schiding, J.K., Wisniewski, S.R., Kelsey, S.F., DeKosky, S.T., Graham, S.H., Marion, D.W., and Ho, C. (1997). Assessment of cerebral blood flow and CO2 reactivity after controlled cortical impact by perfusion magnetic resonance imaging using arterial spin-labeling in rats. J. Cereb. Blood Flow Metab. 17, 865-874.
20. Gallyas, F., Pat, J., Farkas, O., Dóczi, T. (2006). The fate of axons subjected to traumatic ultrastructural (neurofilament) compaction: An electron-microscopic study. Acta neuropathologica 111, 229-237.
21. Gentleman, S.M., Nash, M.J., Sweeting, C.J., Graham, D.I., and Roberts, G.W. (1993). Beta-Amyloid precursor protein (beta APP) as a marker for axonal injury after head injury. Neurosci. Lett. 160, 139-144.
22. Ginsberg, M.D., Zhao, W., Belayev, L., Alonso, O.F., Liu, Y., Loor, J.Y., and Busto, R. (2001). Diminution of metabolism/ blood flow uncoupling following traumatic brain injury in rats in response to high-dose human albumin treatment. J. Neurosurg. 94, 499-509.
23. Greer, J.E., McGinn, M.J., and Povlishock, J.T. (2011). Diffuse traumatic axonal injury in the mouse induces atrophy, c-Jun activation, and axonal outgrowth in the axotomized neuronal population. J. Neurosci. 30, 5089-5105.
24. Grady, M.S., McLaughlin, M.R., Christman, C.W., Valadka, A.B., Fligner, C.L., and Povlishock, J.T. (1993). The use of antibodies targeted against the neurofilament subunits for the detection of diffuse axonal injury in humans. J. Neuropathol. Exp. Neurol. 52, 143-152.
25. Hamm, R.J., Temple, M.D., Pike, B.R., and Ellis, E.F. (1996). The effect of postinjury administration of polyethylene glycolconjugated superoxide dismutase (pegorgotein, Dismutec) or lidocaine on behavioral function following fluid-percussion brain injury in rats. J. Neurotrauma 13, 325-332.
26. Harris, N.G., Lythgoe, M.F., Thomas, D.L., and Williams, S.R. (2001). Cerebrovascular reactivity following focal brain ischemia in the rat: A functional magnetic resonance imaging study. Neuroimage 13, 339-350.
27. Harris, N.G., Hovda, D.A., and Sutton, R.L. (2009). Acute deficits in transcallosal connectivity endure chronically after experimental brain injury in the rat: A DTI tractography study. J. Neurotrauma 26, A37 (Abstract)
28. Harris, N.G., Zilkha, E., Houseman, J., Symms, M.R., Obrenovitch, T.P., and Williams, S.R. (2000). The relationship between the apparent diffusion coefficient measured by magnetic resonance imaging, anoxic depolarization, and glutamate efflux during experimental cerebral ischemia. J. Cereb. Blood Flow Metab. 20, 28-36.
29. Hossmann, K.A. (1994). Viability thresholds and the penumbra of focal ischemia. Ann. Neurol. 36, 557-565.
30. Ingvar, M., Eriksson, L., Rogers, G.A., Stone-Elander, S., and Widen, L. (1991). Rapid feasibility studies of tracers for positron emission tomography: High-resolution PET in small animals with kinetic analysis. J. Cereb. Blood Flow Metab. 11, 926-931.
31. Kelley, B.J., Farkas, O., Lifshitz, J, and Povlishock, J.T. (2006). Traumatic axonal injury in the perisomatic domain triggers ultrarapid secondary axotomy and Wallerian degeneration. Exp. Neurol. 198, 350-360.
32. Kelly, D.F., Lee, S.M., Pinanong, P.A., and Hovda, D.A. (1997). Paradoxical effects of acute ethanolism in experimental brain injury. J .Neurosurg. 86, 876-882.
33. Kelly, D.F., Kozlowski, D.A., Haddad, E., Echiverri, A., Hovda, D.A., and Lee, S.M. (2000). Ethanol reduces metabolicuncoupling following experimental head injury. J. Neurotrauma 17, 261-272.
34. Kochanek, P.M., Marion, D.W., Zhang, W., Schiding, J.K., White, M., Palmer, A.M., Clark, R.S., O'Malley, M.E., Styren, S.D., and Ho, C. (1995). Severe controlled cortical impact in rats: Assessment of cerebral edema, blood flow, and contusion volume. J. Neurotrauma 12, 1015-1025.
35. Lear, J.L., and Ackermann, R.F. (1989). Regional comparison of the lumped constants of deoxyglucose and fluorodeoxyglucose. Metab. Brain Dis. 4, 95-104.
36. Marion, D.W., Darby, J., and Yonas, H. (1991). Acute regional cerebral blood flow changes caused by severe head injuries. J. Neurosurg. 74, 407-414.
37. Marion, D.W., and White, M.J. (1996). Treatment of experimental brain injury with moderate hypothermia and 21-Aminosteroids. J. Neurotrauma 13, 139-147.
38. Marklund, N., Sihver, S., Langstrom, B., Bergstrom, M., and Hillered, L. (2002). Effect of traumatic brain injury and nitrone radical scavengers on relative changes in regional cerebral blood flow and glucose uptake in rats. J. Neurotrauma 19, 1139-1153.
39. Marmarou, C.R., and Povlishock, J.T. (2006). Administration of the immunophilin ligand FK506 differentially attenuates neurofilament compaction and impaired axonal transport in injured axons following diffuse traumatic brain injury. Exp. Neurol. 197, 353-362. Epub 2005 Nov 17.
40. Marmarou, C.R., Walker, S.A., Lewis, C.L., and Povlishock, J.T. (2005). quantitative analysis of the relationship between intraaxonal neurofilament compaction and impaired axonal transport following diffuse traumatic brain injury. J. Neurotrauma 10, 1066-1080.
41. Martin, N.A., Patwardhan, R.V., Alexander, M.J., Africk, C.Z., Lee, J.H., Shalmon, E., Hovda, D.A., and Becker, D.P. (1997). Characterization of cerebral hemodynamic phases following severe head trauma: Hypoperfusion, hyperemia, and vasospasm. J. Neurosurg. 87, 9-19.
42. Maxwell, W.L., Kosanlavit, R., McCreath, B.J., Reid, O., and Graham, D.I. (1999). Freeze-fracture and cytochemical evidence for structural and functional alteration in the axolemma and myelin sheath of adult guinea pig optic nerve fibers after stretch injury. J. Neurotrauma 16, 273-284.
43. Maxwell, W.L., McCreath, B.J., Graham, D.I., and Gennarelli, T.A. (1995). Cytochemical evidence for redistribution of membrane pump calcium-ATPase and ecto-Ca-ATPase activity, and calcium influx in myelinated nerve fibres of the optic nerve after stretch injury. J. Neurocytol. 24, 925-942.
44. Maxwell, W.L., Povlishock, J.T., and Graham, D.L. (1997). A mechanistic analysis of nondisruptive axonal injury: A review. J. Neurotrauma 14, 419-440.
45. Maxwell, W.L., Watt, C., Graham, D.I., and Gennarelli, T.A. (1993). Ultrastructural evidence of axonal shearing as a result of lateral acceleration of the head in non-human primates. Acta Neuropathol. (Berl.) 86, 136-144.
46. Moro, N., and Sutton, R.L. (2010). Beneficial effects of sodium or ethyl pyruvate after traumatic brain injury in the rat. Exp. Neurol. 225, 391-401.
47. Muir, J.K., Tynan, M., Caldwell, R., and Ellis, E.F. (1995). Superoxide dismutase improves posttraumatic cortical blood flow in rats. J. Neurotrauma 12, 179-188.
48. Nixon, R.A., Lewis, S.E., Mercken, M., and Sihag, R.K. (1994b). [32P]orthophosphate and [35S]methionine label separate pools of neurofilaments with markedly different axonal transport kinetics in mouse retinal ganglion cells in vivo. Neurochem. Res. 19, 1445-1453.
49. Nixon, R.A., Paskevich, P.A., Sihag, R.K., and Thayer, C.Y. (1994a). Phosphorylation on carboxyl terminus domains of neurofilament proteins in retinal ganglion cell neurons in vivo: Influences on regional neurofilament accumulation, interneurofilament spacing, and axon caliber. J. Cell Biol. 126, 1031-1046.
50. Okonkwo, D.O., Pettus, E.H., Moroi, J., and Povlishock, J.T. (1998). Alteration of the neurofilament sidearm and its relation to neurofilament compaction occurring with traumatic axonal injury. Brain Res. 784, 1-6.
51. Paxinos, G., and Watson, C. (1997). The Rat Brain in Stereotaxic Coordinates, 3rd ed. Academic Press.
52. Pettus, E.H., and Povlishock, J.T. (1996). Characterization of a distinct set of intra-Axonal ultrastructural changes associated with traumatically induced alteration in axolemmal permeability. Brain Res. 722, 1-11.
53. Povlishock, J.T., and Pettus, E.H. (1996). Traumatically induced axonal damage: Evidence for enduring changes in axolemmal permeability with associated cytoskeletal change. Acta Neurochir. Suppl. (Wien.) 66, 81-86.
54. Reeves, T.M., Phillips, L.L., Lee, N.N., and Povlishock, J.T. (2007). Preferential neuroprotective effect of tacrolimus (FK506) on unmyelinated axons following traumatic brain injury. Brain Res. 1154, 225-236.
55. Richards, H.K., Simac, S., Piechnik, S., and Pickard, J.D. (2001). Uncoupling of cerebral blood flow and metabolism after cerebral contusion in the rat. J. Cereb. Blood Flow Metab. 21, 779-781.
56. Robertson, C.S., Contant, C.F., Gokaslan, Z.L., Narayan, R.K., and Grossman, R.G. (1992). Cerebral blood flow, arteriovenous oxygen difference, and outcome in head injured patients. J. Neurol. Neurosurg. Psychiatry 55:, 594-603.
57. Rockswold, S.B., Rockswold, G.L., Vargo, J.M., Erickson, C.A., Sutton, R.L., Bergman, T.A., and Biros, M.H. (2001). Effects of hyperbaric oxygen therapy on cerebral metabolism and intracranial pressure in severely brain injured patients. J. Neurosurg. 94, 403-411.
58. Saatman, K.E., Abai, B., Grosvenor, A., Vorwerk, C.K., Smith, D.H., and Meaney, D.F. (2003). Traumatic axonal injury results in biphasic calpain activation and retrograde transport impairment in mice. J. Cereb. Blood Flow Metab. 23, 34-42.
59. Saatman, K.E., Bozyczko-Coyne, D., Marcy, V., Siman, R., and McIntosh, T.K. (1996). Prolonged calpain-mediated spectrin breakdown occurs regionally following experimental brain injury in the rat. J. Neuropathol. Exp. Neurol. 55, 850-860.
60. Schurr, A., Miller, J.J., Payne, R.S., and Rigor, B.M. (1999). An increase in lactate output by brain tissue serves to meet the energy needs of glutamate-Activated neurons. J. Neurosci. 19, 34-39.
61. Singleton, R.H., Zhu, J., Stone, J.R., and Povlishock, J.T. (2002). Traumatically induced axotomy adjacent to the soma does not result in acute neuronal death. J. Neurosci. 22, 791-802.
62. Stone, J.R, Okonkwo, D.O., Dialo, A.O., Rubin, D.G., Mutlu, L.K., Povlishock, J.T., and Helm, G.A. (2004). Impaired axonal transport and altered axolemmal permeability occur in distinct populations of damaged axons following traumatic brain injury. Exp. Neurol. 190, 59-69.
63. Stone, J.R., Singleton, R.H., and Povlishock, J.T. (2000). Antibodies to the C-terminus of the beta-Amyloid precursor protein (APP): A site specific marker for the detection of traumatic axonal injury. Brain Res. 871, 288-302.
64. Sunami, K., Nakamura, T., Ozawa, Y., Kubota, M., Namba, H., and Yamaura, A. (1989). Hypermetabolic state followingexperimental head injury. Neurosurg. Rev. 12(Suppl. 1), 400-411.
65. Sutton, R.L., Hovda, D.A., Adelson, P.D., Benzel, E.C., and Becker, D.P. (1994). Metabolic changes following cortical contusion: Relationships to edema and morphological changes. Acta Neurochir. Suppl. (Wien.) 60, 446-448.
66. Yamakami, I., and McIntosh, T.K. (1991). Alterations in regional cerebral blood flow following brain injury in the rat. J. Cereb. Blood Flow Metab. 11, 655-660.
67. Yang, J.T., Chang, C.N., Lee, T.H., Lin, T.N., Hsu, J.C., Hsu, Y.H., and Wu, J.H. (2001). Hyperbaric oxygen treatment decreases post-ischemic neurotrophin-3 mRNA down-regulation in the rat hippocampus. Neuroreport 12, 3589-3592.
68. Yoshino,A.,Hovda, D.A.,Kawamata,T.,Katayama, Y., andBecker, D.P. (1991). Dynamic changes in local cerebral glucose utilization following cerebral conclusion in rats: Evidence of a hyper- and subsequent hypometabolic state. Brain Res. 561, 106-119.
69. Zhao, W., Alonso, O.F., Loor, J.Y., Busto, R., and Ginsberg, M.D. (1999). Influence of early posttraumatic hypothermia therapy on local cerebral blood flow and glucose metabolism after fluid-percussion brain injury. J. Neurosurg. 90, 510-519.