Post-injury administration of mitochondrial uncouplers increases tissue sparing and improves behavioral outcome following traumatic brain injury in rodents

Journal of Neurotrauma

Volumn 24, Issue 5, 2007, Pages 798-811

  Pandya, Jignesh D ^a   Pauly, James R ^a,b   Nukala, Vidya N ^a   Sebastian, Andrea H ^a   Day, Kristen M ^a   Korde, Amit S ^a   Maragos, William F ^a   Hall, Edward D ^a   Sullivan, Patrick G ^a,c  

^a UNIVERSITY OF KENTUCKY   (United States)

^b University of Kentucky   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

2,4 dinitrophenol; Carbonyl cyanide 4 trifluoromethoxy phenylhydrazone; Cortical contusion; Mitochondrial bioenergetics; Mitochondrial uncoupling; Reactive oxygen species

Indexed keywords

2,4 DINITROPHENOL; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOENERGY; BRAIN DAMAGE; BRAIN INJURY; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EXCITOTOXICITY; LONG TERM CARE; MALE; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NEUROPROTECTION; NONHUMAN; RAT; STATISTICAL SIGNIFICANCE;

2,4-DINITROPHENOL; ANIMALS; BRAIN; BRAIN INJURIES; CALCIUM SIGNALING; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; CELL DEATH; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; HOMEOSTASIS; MALE; MITOCHONDRIA; NERVE DEGENERATION; NEURONS; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; TREATMENT OUTCOME; UNCOUPLING AGENTS;

EID: 34249111082     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2006.3673     Document Type: Article

References (59)

1. AMARAL, D., and WITTER, M. (1995). Hippocampal formation, in: The Rat Nervous System. G. Paxinos (ed), Academic Press: New York, pps. 443-493.
2. ANDERSON, K.J., MILLER, K.M., FUGACCIA, I., et al. (2005). Regional distribution of Fluro-Jade B staining in the hippocampus following traumatic brain injury. Exp. Neurol. 193, 125-130.
3. ANDERSON, M.F., and SIMS, N.R. (2000). Improved recovery of highly enriched mitochondrial fractions from small brain tissue samples. Brain Res. Brain Res. Protoc. 5, 95-101.
4. BALDWIN, S.A., GIBSON, T., CALLIHAN, C.T., et al. (1997). Neuronal cell loss in the CA3 subfield of the hippocampus following cortical contusion utilizing the optical disector method for cell counting. J. Neurotrauma 14, 385-398.
5. BILLUPS, B., and FORSYTHE, I.D. (2002). Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J. Neurosci. 22, 5840-5847.
6. BRAUGHLER, J.M., and HALL, E.D. (1992). Involvement of lipid peroxidation in CNS injury. J. Neurotrauma 9, Suppl 1, S1-S7.
7. BRAUGHLER, J.M., DUNCAN, L.A., and CHASE, R.L. (1985). Interaction of lipid peroxidation and calcium in the pathogenesis of neuronal injury. Cent. Nerv. Syst. Trauma 2, 269-283.
8. BROWN, M.R., SULLIVAN, P.G., DORENBOS, K.D., et al. (2004). Nitrogen disruption of synaptoneurosomes: an alternative method to isolate brain mitochondria. J. Neurosci. Methods 137, 299-303.
9. BRUSTOVETSKY, N., BRUSTOVETSKY, T., JEMMERSON, R., et al. (2002). Calcium-induced cytochrome c release from CNS mitochondria is associated with the permeability transition and rupture of the outer membrane. J. Neurochem. 80, 207-218.
10. CHALMERS, S., and NICHOLLS, D.G. (2003). The relationship between free and total calcium concentrations in the matrix of liver and brain mitochondria. J. Biol. Chem. 278, 19062-19070.
11. COOPER, P. (1985), Delayed brain injury: secondary insults, in: Central Nervous System Trauma Status Report. J. Povlishhock and D. Becker (eds), National Institutes of Health: Washington, DC, pps. 217-282.
12. DUGAN, L.L., SENSI, S.L., CANZONIERO, L.M., et al. (1995). Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J. Neurosci. 15, 6377-6388.
13. FADEN, A.I. (1993). Experimental neurobiology of central nervous system trauma. Crit. Rev. Neurobiol. 7, 175-186.
14. FADEN, A.I., DEMEDIUK, P., PANTER, S.S., et al. (1989). The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244, 798-800.
15. HALL, E.D., and SULLIVAN, P.G. (2004). Preserving function in acute nervous system injury, in: Neuroscience, Molecular Medicine and the Therapeutic Transfomation of Neurology S.G. Waxman (ed), Elsevier/Academic Press: San Diego, pps. 35-59.
16. ICHAS, F., and MAZAT, J.P. (1998). From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim. Biophys. Acta 1366, 33-50.
17. 2+ induces permeability transition pore opening and release of pro-apoptotic peptides from neuronal mitochondria. J. Biol. Chem. 276, 47524-47529.
18. KIM-HAN, J.S., REICHERT, S.A., QUICK, K.L., et al. (2001). BMCP1: a mitochondrial uncoupling protein in neurons which regulates mitochondrial function and oxidant production. J. Neurochem. 79, 658-668.
19. KIRICHOK, Y., KRAPIVINSKY, G., and CLAPHAM, D.E. (2004). The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427, 360-364.
20. KORDE, A.S., SULLIVAN, P.G., and MARAGOS, W.F. (2005a). The uncoupling agent 2,4-dinitrophenol improves mitochondrial homeostasis following striatal quinolinic acid injections. J. Neurotrauma 22, 1142-1149.
21. KORDE, A.S., PETTIGREW, L.C., CRADDOCK, S.D., et al. (2005b). The mitochondrial uncoupler 2,4-dinitrophenol attenuates tissue damage and improves mitochondrial homeostasis following transient focal cerebral ischemia. J. Neurochem. 94, 1676-1684.
22. KURT, T.L., ANDERSON, R., PETTY, C., et al. (1986). Dinitrophenol in weight loss: the poison center and public health safety. Vet. Hum. Toxicol. 28, 574-575.
23. LI, L.X., SKORPEN, F., EGEBERG, K., et al. (2001). Uncoupling protein-2 participates in cellular defense against oxidative stress in clonal beta-cells. Biochem. Biophys. Res. Commun. 282, 273-277.
24. LIFSHITZ, J., SULLIVAN, P.G., HOVDA, D.A., et al. (2004). Mitochondrial damage and dysfunction in traumatic brain injury. Mitochondria 1, 705-713.
25. LIFSHITZ, J., FRIBERG, H., NEUMAR, R.W., et al. (2003). Structural and functional damage sustained by mitochondria after traumatic brain injury in the rat: evidence for differentially sensitive populations in the cortex and hippocampus. J. Cereb. Blood Flow Metab. 23, 219-231.
26. LIU, Y., FISKUM, G., and SCHUBERT, D. (2002). Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 80, 780-787.
27. MARAGOS, W.F., ROCKlCH, K.T., DEAN, J.J., et al. (2003). Pre- or post-treatment with the mitochondrial uncoupler 2,4-dinitrophenol attenuates striatal quinolinate lesions. Brain Res. 966, 312-316.
28. MATTIASSON, G., and SULLIVAN, P.G. (2006). The emerging roles of UCP2 in health and disease. Antioxidants Redox Signaling 8, 1-38.
29. MATTIASSON, G., SHAMLOO, M., GIDO, G., et al. (2003). Uncoupling protein-2 prevents neuronal death and diminishes brain dysfunction after stroke and brain trauma. Nat. Med. 9, 1062-1068.
30. McCULLERS, D.L., SULLIVAN, P.G., SCHEFF, S.W., et al. (2002). Mifepristone protects CA1 hippocampal neurons following traumatic brain injury in rat. Neuroscience 109, 219-230.
31. MORRIS, R. (1984). Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47-60.
32. NICHOLLS, D.G., and BUDD, S.L. (1998a). Mitochondria and neuronal glutamate excitotoxicity. Biochim. Biophys. Acta 1366, 97-112.
33. NICHOLLS, D.G., and BUDD, S.L. (1998b). Neuronal excitotoxicity: the role of mitochondria. Biofactors 8, 287-299.
34. PIVOVAROVA, N.B., POZZO-MILLER, L.D., HONG-PAISAN, J., et al. (2002). Correlated calcium uptake and release by mitochondria and endoplasmic reticulum of CA3 hippocampal dendrites after afferent synaptic stimulation. J. Neurosci. 22, 10653-10661.
35. PIVOVAROVA, N.B., NGUYEN, H.V., WINTERS, C.A., et al. (2004). Excitotoxic calcium overload in a subpopulation of mitochondria triggers delayed death in hippocampal neurons. J. Neurosci. 24, 5611-5622.
36. REYNOLDS, I.J., and HASTINGS, T.G. (1995). Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J. Neurosci. 15, 3318-3327.
37. RIZZUTO, R., BERNARDI, P., and POZZAN, T. (2000). Mitochondria as all-round players of the calcium game. J. Physiol. 529, 37-47.
38. RIZZUTO, R., PINTON, P., BRINI, M., et al. (1999). Mitochondria as biosensors of calcium microdomains. Cell Calcium 26, 193-199.
39. ROTHMAN, S.M., and OLNEY, J.W. (1995). Excitotoxicity and the NMDA receptor - still lethal after eight years. Trends Neurosci. 18, 57-58.
40. SCHEFF, S.W., and SULLIVAN, P.G. (1999). Cyclosporin A significantly ameliorates cortical damage following experimental traumatic brain injury in rodents. J. Neurotrauma 16, 783-792.
41. SCHEFF, S.W., BALDWIN, S.A., BROWN, R.W., et al. (1997). Morris water maze deficits in rats following traumatic brain injury: lateral controlled cortical impact. J. Neurotrauma 14, 615-627.
42. SENGPIEL, B., PREIS, E., KRIEGLSTEIN, J., et al. (1998). NMDA-induced superoxide production and neurotoxicity in cultured rat hippocampal neurons: role of mitochondria. Eur. J. Neurosci. 10, 1903-1910.
43. 2+ pools. Proc. Natl. Acad. Sci. USA 100, 6157-6162.
44. SIESJO, B.K., KATSURA, K., ZHAO, Q., et al. (1995). Mechanisms of secondary brain damage in global and focal ischemia: a speculative synthesis. J. Neurotrauma 12, 943-956.
45. SMITH, S.L., ANDRUS, P.K., ZHANG, J.R., et al. (1994). Direct measurement of hydroxyl radicals, lipid peroxidation, and blood-brain barrier disruption following unilateral cortical impact head injury in the rat. J. Neurotrauma 11, 393-404.
46. STARKOV, A.A., and FISKUM, G. (2003). Regulation of brain mitochondrial H2O2 production by membrane potential and NAD(P)H redox state. J. Neurochem. 86, 1101-1107.
47. STARKOV, A.A., POLSTER, B.M., and FISKUM, G. (2002). Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax. J. Neurochem. 83, 220-228.
48. STOUT, A.K., RAPHAEL, H.M., KABTEREWUCZ, B.I., et al. (1998). Glutamate-induced neuron death requires mitochondrial calcium uptake. Nat. Neurosci. 1, 366-373.
49. SULLIVAN, P.G., THOMPSON, M.B., and SCHEFF, S.W. (1999). Cyclosporin A attenuates acute mitochondrial dysfunction following traumatic brain injury. Exp. Neurol. 160, 226-234.
50. SULLIVAN, P.G., KELLER, J.N., MATTSON, M.P., et al. (1998). Traumatic brain injury alters synaptic homeostasis: implications for impaired mitochondrial and transport function. J. Neurotrauma 15, 789-798.
51. SULLIVAN, P.G., GEIGER, J.D., MATTSON, M.P., et al. (2000). Dietary supplement creatine protects against traumatic brain injury. Ann. Neurol. 48, 723-729.
52. SULLIVAN, P.G., KELLER, J.N., BUSSEN, W.L., et al. (2002). Cytochrome c release and caspase activation after traumatic brain injury. Brain Res. 949, 88-96.
53. SULLIVAN, P.G., SPRINGER, J.E., HALL, E.D., et al. (2004a). Mitochondrial uncoupling as a therapeutic target following neuronal injury. J. Bioenerg. Biomembr. 36, 353-356.
54. SULLIVAN, P.G., RABCHEVSKY, A.G., WALDMEIER, P.C., et al. (2005). Mitochondrial permeability transition in CNS trauma: cause or effect of neuronal cell death? J. Neurosci. Res. 79, 231-239.
55. SULLIVAN, P.G., DUBE, C., DORENBOS, K.D., et al. (2003). Mitochondrial uncoupling protein-2 protects the immature brain from excitotoxic neuronal death. Ann. Neurol. 53, 711-717.
56. SULLIVAN, P.G., RIPPY, N.A., DORENBOS, K.D., et al. (2004b). The ketogenic diet increases mitochondrial uncoupling protein levels and activity in mouse hippocampus. Ann. Neurol. 55, 576-580.
57. SULLIVAN, P.G., RABCHEVSKY, A.G., KELLER, J.N., et al. (2004c). Intrinsic differences in brain and spinal cord mitochondria: implication for therapeutic interventions. J. Comp. Neurol. 474, 524-534.
58. WHITE, R.J., and REYNOLDS, I.J. (1996). Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J. Neurosci. 16, 5688-5697.
59. XIONG, Y., GU, Q., PETERSON, P.L., et al. (1997). Mitochondrial dysfunction and calcium perturbation induced by traumatic brain injury. J. Neurotrauma 14, 23-34.