Early and sustained alterations in cerebral metabolism after traumatic brain injury in immature rats

Journal of Neurotrauma

Volumn 25, Issue 6, 2008, Pages 603-614

  Casey, Paula A ^a   McKenna, Mary C ^a   Fiskum, Gary ^a   Saraswati, Manda ^a   Robertson, Courtney L ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Development; Lactate; Mitochondria; N Acetyl aspartate; NMR spectroscopy

Indexed keywords

ALANINE; CHOLINE; CREATININE; LACTIC ACID; N ACETYLASPARTIC ACID;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN METABOLISM; CONTROLLED STUDY; GLYCOLYSIS; HEMISPHERE; IMMATURITY; NONHUMAN; PARIETAL LOBE; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; TRAUMATIC BRAIN INJURY;

AGING; ALANINE; ANIMALS; ANIMALS, NEWBORN; ASPARTIC ACID; BRAIN; BRAIN INJURIES; CELL RESPIRATION; CHOLINE; CREATINE; DISEASE PROGRESSION; ENERGY METABOLISM; GLYCOLYSIS; LACTIC ACID; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MITOCHONDRIA; NERVE DEGENERATION; OXIDATIVE PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 46349108591     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2007.0481     Document Type: Article

References (73)

1. 1H-Magnetic resonance spectroscopy-determined cerebral lactate and poor neurological outcomes in children with central nervous system disease. Ann. Neurol. 41, 470-481.
2. Ashwal, S., Holshouser, B.A., Shu, S.K., Simmons, P.L., Perkin, R.M., Tomasi, L.G., Knierim, D.S., Sheridan, C., Craig, K., Andrews, G.H., and Hinshaw, D.B. (2000). Predictive value of proton magnetic resonance spectroscopy in pediatric closed head injury. Pediatr. Neurol. 23, 114-125.
3. Ashwal, S., Holshouser B., Tong K., Serna T., Osterdock R., Gross M., and Kido D. (2004). Proton MR spectroscopy detected glutamate/glutamine is increased in children with traumatic brain injury. J. Neurotrauma 21, 1539-1552.
4. Ashwal, S., Babikian, T., Gardner-Nichols, J., Freier, M.C., Tong, K.A., and Holshouser, B.A. (2006a). Susceptibility-weighted imaging and proton magnetic resonance spectroscopy in assessment of outcome after pediatric traumatic brain injury. Arch. Phys. Med. Rehabil. 87, S50-S58.
5. Ashwal, S., Holshouser, B.A., and Tong, K.A. (2006b). Use of advanced neuroimaging techniques in the evaluation of pediatric traumatic brain injury. Dev. Neurosci. 28, 309-326.
6. Barkovich, A.J., Baranski, K., Vigneron, D., Partridge, J.C., Hallam, D.K., Hajnal, B.L., and Ferriero, D.M. (1999). Proton MR spectroscopy for the evaluation of brain injury in asphyxiated, term neonates. AJNR Am. J. Neuroradiol. 20, 1399-1405.
7. Bartnik, B.L., Sutton, R.L., Fukushima, M., Harris, N.G., Hovda, D.A., and Lee, S.M. (2005). Upregulation of pentose phosphate pathway and preservation of tricarboxylic acid cycle flux after experimental brain injury. J. Neurotrauma 22, 1052-1065.
8. 1H NMR study of cerebral development in the rat. NMR Biomed. 2, 225-229.
9. Bogaert, Y.E., Sheu, K.F., Hof, P.R., Brown, A.M., Blass, J.P., Rosenthal, R.E., and Fiskum, G. (2000). Neuronal subclass-selective loss of pyruvate dehydrogenase immunoreactivity following canine cardiac arrest and resuscitation. Exp. Neurol. 161, 115-126.
10. Brenner, T., Freier, M.C., Holshouser, B.A., Burley, T., and Ashwal, S. (2003). Predicting neuropsychologic outcome after traumatic brain injury in children. Pediatr. Neurol. 28, 104-114.
11. Brooks, W.M., Stidley, C.A., Petropoulos, H., Jung, R.E., Weers, D.C., Friedman, S.D., Barlow, M.A., Sibbitt, W.L., Jr., and Yeo, R.A. (2000). Metabolic and cognitive response to human traumatic brain injury: a quantitative proton magnetic resonance study. J. Neurotrauma 17, 629-640.
12. Brooks, W.M., Friedman, S.D., and Gasparovic, C. (2001). Magnetic resonance spectroscopy in traumatic brain injury. J. Head Trauma Rehabil. 16, 149-164.
13. 1H magnetic resonance spectroscopy of rat brain extracts compared with chromatographic methods. Neurochem. Res. 15, 1009-1016.
14. 1H magnetic resonance spectroscopy. Invest. Radiol. 30, 502-506.
15. Clark, J.B. (1998). N-Acetyl aspartate: a marker for neuronal loss or mitochondrial dysfunction. Dev. Neurosci. 20, 271-276.
16. Cohen, Y., Sanada, T., Pitts, L.H., Chang, L.H., Nishimura, M.C., Weinstein, P.R., Litt, L., and James, T.L. (1991). Surface coil spectroscopic imaging: time and spatial evolution of lactate production following fluid percussion brain injury. Magn. Reson. Med. 17, 225-236.
17. D'Adamo, A.F., Jr., and Yatsu, F.M. (1966). Acetate metabolism in the nervous system. N-Acetyl-L-aspartic acid and the biosynthesis of brain lipids. J. Neurochem. 13, 961-965.
18. Davies, S.E., Newcombe, J., Williams, S.R., McDonald, W.I., and Clark, J.B. (1995). High-resolution proton NMR spectroscopy of multiple sclerosis lesions. J. Neurochem. 64, 742-748.
19. Dienel, G.A., and Cruz, N.F. (2003). Neighborly interactions of metabolically-activated astrocytes in vivo. Neurochem. Int. 43, 339-354.
20. Federico, F., Simone, I.L., Lucivero, V., De Mari, M., Giannini, P., Iliceto, G., Mezzapesa, D.M., and Lamberti, P. (1997). Proton magnetic resonance spectroscopy in Parkinson's disease and progressive supranuclear palsy. J. Neurol. Neurosurg. Psychiatry 62, 239-242.
21. Friedman, S.D., Brooks, W.M., Jung, R.E., Chiulli, S.J., Sloan, J.H., Montoya, B.T., Hart, B.L., and Yeo, R.A. (1999). Quantitative proton MRS predicts outcome after traumatic brain injury. Neurology 52, 1384-1391.
22. Garnett, M.R., Blamire, A.M., Corkill, R.G., Cadoux-Hudson, T.A., Rajagopalan, B., and Styles, P. (2000). Early proton magnetic resonance spectroscopy in normal-appearing brain correlates with outcome in patients following traumatic brain injury. Brain 123, 2046-2054.
23. Garnett, M.R., Corkill, R.G., Blamire, A.M., Rajagopalan, B., Manners, D.N., Young, J.D., Styles, P., and Cadoux-Hudson, T.A. (2001). Altered cellular metabolism following traumatic brain injury: a magnetic resonance spectroscopy study. J. Neurotrauma 18, 231-240.
24. Gasparovic, C., Arfai, N., Smid, N., and Feeney, D.M. (2001). Decrease and recovery of N-acetylaspartate/creatine in rat brain remote from focal injury. J. Neurotrauma 18, 241-246.
25. Godbolt, A.K., Waldman, A.D., MacManus, D.G., Schott, J.M., Frost, C., Cipolotti, L., Fox, N.C., and Rossor, M.N. (2006). MRS shows abnormalities before symptoms in familial Alzheimer disease. Neurology 66, 718-722.
26. 1H-NMR spectroscopy. J. Neurochem. 68, 305-312.
27. Hawley, C.A. (2003). Reported problems and their resolution following mild, moderate and severe traumatic brain injury amongst children and adolescents in the UK. Brain Inj. 17, 105-129.
28. Hazany, S., Hesselink, J.R., Healy, J.F., and Imbesi, S.G. (2007). Utilization of glutamate/creatine ratios for proton spectroscopic diagnosis of meningiomas. Neuroradiology 49, 121-127.
29. Holshouser, B.A., Ashwal, S., Luh, G.Y., Shu, S., Kahlon, S., Auld, K.L., Tomasi, L.G., Perkin, R.M., and Hinshaw, D.B., Jr. (1997). Proton MR spectroscopy after acute central nervous system injury: outcome prediction in neonates, infants, and children. Radiology 202, 487-496.
30. Holshouser, B.A., Tong, K.A., and Ashwal, S. (2005). Proton MR spectroscopic imaging depicts diffuse axonal injury in children with traumatic brain injury. AJNR Am. J. Neuroradiol. 26, 1276-1285.
31. Holshouser, B.A., Tong, K.A., Ashwal, S., Oyoyo, U., Ghamsary, M., Saunders, D., and Shutter, L. (2006). Prospective longitudinal proton magnetic resonance spectroscopic imaging in adult traumatic brain injury. J. Magn. Reson. Imaging 24, 33-40.
32. Hunter, J.V., Thornton, R.J., Wang, Z.J., Levin, H.S., Roberson, G., Brooks, W.M., and Swank, P.R. (2005). Late proton MR spectroscopy in children after traumatic brain injury: correlation with cognitive outcomes. AJNR Am. J. Neuroradiol. 26, 482-488.
33. Inao, S., Marmarou, A., Clarke, G.D., Andersen, B.J., Fatouros, P.P., and Young, H.F. (1988). Production and clearance of lactate from brain tissue, cerebrospinal fluid, and serum following experimental brain injury. J. Neurosurg. 69, 736-744.
34. Kawamata, T., Katayama, Y., Hovda, D.A., Yoshino, A., and Becker, D.P. (1995). Lactate accumulation following concussive brain injury: the role of ionic fluxes induced by excitatory amino acids. Brain Res. 674, 196-204.
35. Keenan, H.T., Hooper, S.R., Wetherington, C.E., Nocera, M., and Runyan, D.K. (2007). Neurodevelopmental consequences of early traumatic brain injury in 3-year-old children. Pediatrics 119, e616-e623.
36. Kochanek, P.M., Clark, R.S., Ruppel, R.A., Adelson, P.D., Bell, M.J., Whalen, M.J., Robertson, C.L., Satchell, M.A., Seidberg, N.A., Marion, D.W., and Jenkins, L.W. (2000). Biochemical, cellular, and molecular mechanisms in the evolution of secondary damage after severe traumatic brain injury in infants and children: Lessons learned from the bedside. Pediatr. Crit. Care Med. 1, 4-19.
37. Kochanek, A.R., Kline, A.E., Gao, W.M., Chadha, M., Lai, Y., Clark, R.S., Dixon, C.E., and Jenkins, L.W. (2006). Gelbased hippocampal proteomic analysis 2 weeks following traumatic brain injury to immature rats using controlled cortical impact. Dev. Neurosci. 28, 410-419.
38. Liu, M.C., Akle, V., Zheng, W., Kitlen, J., O'Steen, B., Larner, S.F., Dave, J.R., Tortella, F.C., Hayes, R.L., and Wang, K.K. (2006). Extensive degradation of myelin basic protein isoforms by calpain following traumatic brain injury. J. Neurochem. 98, 700-712.
39. Lopez-Villegas, D., Lenkinski, R.E., Wehrli, S.L., Ho, W.Z., and Douglas, S.D. (1995). Lactate production by human monocytes/macrophages determined by proton MR spectroscopy. Magn. Reson. Med. 34, 32-38.
40. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
41. Makoroff, K.L., Cecil, K.M., Care, M., and Ball, W.S., Jr. (2005). Elevated lactate as an early marker of brain injury in inflicted traumatic brain injury. Pediatr. Radiol. 35, 668-676.
42. Malik, G.K., Pandey, M., Kumar, R., Chawla, S., Rathi, B., and Gupta, R.K. (2002). MR imaging and in vivo proton spectroscopy of the brain in neonates with hypoxic ischemic encephalopathy. Eur. J. Radiol. 43, 6-13.
43. Marino, S., Zei, E., Battaglini, M., Vittori, C., Buscalferri, A., Bramanti, P., Federico, A., and De Stefano, N. (2007). Acute metabolic brain changes following traumatic brain injury and their relevance to clinical severity and outcome. J. Neurol. Neurosurg. Psychiatry 78, 501-507.
44. Martin, E., Rosenthal, R.E., and Fiskum, G. (2005). Pyruvate dehydrogenase complex: metabolic link to ischemic brain injury and target of oxidative stress. J. Neurosci. Res. 79, 240-247.
45. 31P nuclear magnetic resonance. J. Neurochem. 49, 1530-1540.
46. McKenna, M.C., Tildon, J.T., Stevenson, J.H., and Hopkins, I.B. (1994). Energy metabolism in cortical synaptic terminals from weanling and mature rat brain: evidence for multiple compartments of tricarboxylic acid cycle activity. Dev. Neurosci. 16, 291-300.
47. McKenna, M.C., Gruetter, R., Sonnewald, U., Waagepetersen, H.S., and Schousboe, A. (2006). Energy metabolism of the brain, in: Basic Neurochemistry. G.J. Siegel, R.W. Albers, S.T. Brady, and D.L. Price (eds), Elsevier Academic Press: Burlington, MA, pps. 531-557.
48. Meijer, A.J., and van Dam, K. (1974). The metabolic significance of anion transport in mitochondria. Biochim. Biophys. Acta 346, 213-244.
49. O'Brien, J., Kla, K.M., Hopkins, I.B., Malecki, E.A., and McKenna, M.C. (2007). Kinetic parameters and lactate dehydrogenase isozyme activities support possible lactate utilization by neurons. Neurochem. Res. 32, 597-607.
50. Opii, W.O., Nukala, V.N., Sultana, R., Pandya, J.D., Day, K.M., Merchant, M.L., Klein, J.B., Sullivan, P.G., and Butterfield, D.A. (2007). Proteomic identification of oxidized mitochondrial proteins following experimental traumatic brain injury. J. Neurotrauma 24, 772-789.
51. 1H NMR spectroscopy. J. Neurotrauma 24, 944-959.
52. Patel, T.B., and Clark, J.B. (1979). Synthesis of N-acetyl-L- aspartate by rat brain mitochondria and its involvement in mitochondrial/ cytosolic carbon transport. Biochem. J. 184, 539-546.
53. Pellerin, L., Pellegri, G., Bittar, P.G., Charnay, Y., Bouras, C., Martin, J.L., Stella, N., and Magistretti, P.J. (1998). Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev. Neurosci. 20, 291-299.
54. Petroff, O.A., Graham, G.D., Blamire, A.M., al Rayess, M., Rothman, D.L., Fayad, P.B., Brass, L.M., Shulman, R.G., and Prichard, J.W. (1992). Spectroscopic imaging of stroke in humans: histopathology correlates of spectral changes. Neurology 42, 1349-1354.
55. Richards, E.M., Rosenthal, R.E., Kristian, T., and Fiskum, G. (2006). Postischemic hyperoxia reduces hippocampal pyruvate dehydrogenase activity. Free Radic. Biol. Med. 40, 1960-1970.
56. Richards, E.M., Fiskum, G., Rosenthal, R.E., Hopkins, I., and McKenna, M.C. (2007). Hyperoxic reperfusion after global ischemia decreases hippocampal energy metabolism. Stroke 38, 1578-1584.
57. Robertson, C.L., Bucci, C.J., and Fiskum, G. (2004). Mitochondrial response to calcium in the developing brain. Brain Res. Dev. Brain Res. 151, 141-148.
58. Robertson, C.L., Soane, L., Siegel, Z.T., and Fiskum, G. (2006). The potential role of mitochondria in pediatric traumatic brain injury. Dev. Neurosci. 28, 432-446.
59. Robertson, C.L., Saraswati, M., and Fiskum, G. (2007). Mitochondrial dysfunction early after traumatic brain injury in immature rats. J. Neurochem. 101, 1248-1257.
60. 1H MRS in acute traumatic brain injury. J. Magn. Reson. Imaging 8, 829-840.
61. 2+ signaling in neuronal mitochondria. J. Neurosci. Res. 85, 3359-3366.
62. Schuhmann, M.U., Stiller, D., Skardelly, M., Bernarding, J., Klinge, P.M., Samii, A., Samii, M., and Brinker, T. (2003). Metabolic changes in the vicinity of brain contusions: a proton magnetic resonance spectroscopy and histology study. J. Neurotrauma 20, 725-743.
63. Serres, S., Bezancon, E., Franconi, J.-M., and Merle, M. (2004). Ex vivo analysis of lactate and glucose metabolism in the rat brain under different states of depressed activity. J. Biol. Chem. 279, 47881-47889.
64. 1H-MRS in perinatal CNS insults. Pediatr. Neurol. 17, 309-318.
65. Shutter, L., Tong, K.A., and Holshouser, B.A. (2004). Proton MRS in acute traumatic brain injury: role for glutamate/glutamine and choline for outcome prediction. J. Neurotrauma 21, 1693-1705.
66. Soustiel, J.F., Glenn, T.C., Shik, V., Boscardin, J., Mahamid, E., and Zaaroor, M. (2005). Monitoring of cerebral blood flow and metabolism in traumatic brain injury. J. Neurotrauma 22, 955-965.
67. Tallan, H.H., Moore, S., and Stein, W.H. (1956). N-Acetyl-L- aspartic acid in brain. J. Biol. Chem. 219, 257-264.
68. Taylor, D.L., Davies, S.E., Obrenovitch, T.P., Doheny, M.H., Patsalos, P.N., Clark, J.B., and Symon, L. (1995). Investigation into the role of N-acetylaspartate in cerebral osmoregulation. J. Neurochem. 65, 275-281.
69. Thomas, S., Prins, M.L., Samii, M., and Hovda, D.A. (2000). Cerebral metabolic response to traumatic brain injury sustained early in development: a 2-deoxy-D-glucose autoradiographic study. J. Neurotrauma 17, 649-665.
70. Viant, M.R., Lyeth, B.G., Miller, M.G., and Berman, R.F. (2005). An NMR metabolomic investigation of early metabolic disturbances following traumatic brain injury in a mammalian model. NMR Biomed. 18, 507-516.
71. Yeo, R.A., Phillips, J.P., Jung, R.E., Brown, A.J., Campbell, R.C., and Brooks, W.M. (2006). Magnetic resonance spectroscopy detects brain injury and predicts cognitive functioning in children with brain injuries. J. Neurotrauma 23, 1427-1435.
72. Yoshino, A., Hovda, D.A., Kawamata, T., Katayama, Y., and Becker, 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.
73. 13C isotopomer analysis of glucose and alanine metabolism reveals cytosolic pyruvate compartmentation as part of energy metabolism in astrocytes. Glia 34, 200-212.