Effects of traumatic brain injury of different severities on emotional, cognitive, and oxidative stress-related parameters in mice

Journal of Neurotrauma

Volumn 27, Issue 10, 2010, Pages 1883-1893

  Schwarzbold, Marcelo L ^a   Rial, Daniel ^b   De Bem, Tatiana ^b   MacHado, Daniele G ^a   Cunha, Mauricio P ^a   Dos Santos, Alessandra A ^a   Dos Santos, Danúbia B ^a   Figueiredo, Cláudia P ^a   Farina, Marcelo ^a   Goldfeder, Eliane M ^a   Rodrigues, Ana Lúcia S ^a   Prediger, Rui D S ^a,b   Walz, Roger ^a,c  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b Hospital Universitario   (Brazil)

^c HOSPITAL GOVERNADOR CELSO RAMOS   (Brazil)

Author keywords

anxiety; depression; learning and memory; oxidative stress; traumatic brain injury

Indexed keywords

GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; AVOIDANCE BEHAVIOR; BEHAVIOR; BRAIN CORTEX; COGNITION; DEPRESSION; EMOTION; FORCED SWIMMING TEST; HISTOPATHOLOGY; LOCOMOTION; MALE; MAZE TEST; MOUSE; NONHUMAN; OXIDATIVE STRESS; TRAUMATIC BRAIN INJURY;

ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; BRAIN INJURIES; CEREBRAL CORTEX; EMOTIONS; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HIPPOCAMPUS; INJURY SEVERITY SCORE; MALE; MICE; MOTOR ACTIVITY; OXIDATIVE STRESS; STATISTICS, NONPARAMETRIC;

EID: 77958175236     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2010.1318     Document Type: Article

References (71)

1. Ansari, M. A., Roberts, K. N., and Scheff, S. W. (2008). A time course of contusion-induced oxidative stress and synaptic proteins in cortex in a rat model of TBI. J. Neurotrauma 25, 513-526.
2. Babcock, A. M., Baker, D. A., and Lovec, R. (1993). Locomotor activity in the ischemic gerbil. Brain Res. 625, 351-354.
3. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
4. Brooks, N., Campsie, L., Symington, C., Beattie, A., and McKinlay, W. (1986). The five year outcome of severe blunt head injury: a relative's view. J. Neurol. Neurosurg. Psychiatry 49, 764-770.
5. Bryant, R. A., O'Donnell, M. L., Creamer, M., McFarlane, A. C., Clark, C. R., and Silove, D. (2010). The psychiatric sequelae of traumatic injury. Am. J. Psychiatry 167, 312-320.
6. Carlberg, I., and Mannervik, B. (1985). Glutathione reductase. Methods Enzymol. 113, 484-490.
7. Carroll, L. J., Cassidy, J. D., Peloso, P. M., Borg, J., von Holst, H., Holm, L., Paniak, C., and Pepin, M. (2004). Prognosis for mild traumatic brain injury: results of the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury. J. Rehabil. Med. 43 Suppl., 84-105.
8. Cernak, I. (2005). Animal models of head trauma. NeuroRx 2, 410-422.
9. Chong, Z. Z., Li, F., and Maiese, K. (2005). Oxidative stress in the brain: novel cellular targets that govern survival during neurodegenerative disease. Prog. Neurobiol. 75, 207-246.
10. Cunha, M. P., Machado, D. G., Bettio, L. E., Capra, J. C., and Rodrigues, A. L. S. (2008). Interaction of zinc with antidepressants in the tail suspension test. Prog. Neuropsychopharmacol. Biol. Psychiatry 32, 1913-1920.
11. Darwish, R. S., Amiridze, N., and Aarabi, B. (2007). Nitrotyrosine as an oxidative stress marker: evidence for involvement in neurologic outcome in human traumatic brain injury. J. Trauma 63, 439-442.
12. D'Ambrosio, R., Maris, D. O., Grady, M. S., Winn, H. R., and Janigro, D. (1998). Selective loss of hippocampal long-term potentiation, but not depression, following fluid percussion injury. Brain Res. 786, 64-79.
13. Dringen, R., Pawlowski, P. G., and Hirrlinger, J. (2005). Peroxide detoxification by brain cells. J. Neurosci. Res. 79, 157-165.
14. Ellman, G. L. (1959). Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82, 70-77.
15. Fan, P., Yamauchi, T., Noble, L. J., and Ferriero, D. M. (2003). Age-dependent differences in glutathione peroxidase activity after traumatic brain injury. J. Neurotrauma 20, 437-445.
16. Farina, M., Brandao, R., de Lara, F. S., Pagliosa, L. B., Soares, F. A., Souza, D. O., and Rocha, J. B. (2003). Profile of nonprotein thiols, lipid peroxidation and delta-aminolevulinate dehydratase activity in mouse kidney and liver in response to acute exposure to mercuric chloride and sodium selenite. Toxicology 184, 179-187.
17. Flierl, M. A., Stahel, P. F., Beauchamp, K. M., Morgan, S. J., Smith, W. R., and Shohami, E. (2009). Mouse closed head injury model induced by a weight-drop device. Nat. Protoc. 4, 1328-1337.
18. Fujimoto, S. T., Longhi, L., Saatman, K. E., Conte, V., Stocchetti, N., and McIntosh, T. K. (2004). Motor and cognitive function evaluation following experimental traumatic brain injury. Neurosci. Biobehav. Rev. 28, 365-378.
19. Gil, S., Caspi, Y., Ben-Ari, I. Z., Koren, D., and Klein, E. (2005). Does memory of a traumatic event increase the risk for posttraumatic stress disorder in patients with traumatic brain injury? A prospective study. Am. J. Psychiatry 162, 963-969.
20. Glaesser, J., Neuner, F., Lutgehetmann, R., Schmidt, R., and Elbert, T. (2004). Posttraumatic stress disorder in patients with traumatic brain injury. BMC Psychiatry 4, 5.
21. Gomez-Hernandez, R., Max, J. E., Kosier, T., Paradiso, S., and Robinson, R. G. (1997). Social impairment and depression after traumatic brain injury. Arch. Phys. Med. Rehabil. 78, 1321-1326.
22. Hall, E. D., Andrus, P. K., and Yonkers, P. A. (1993). Brain hydroxyl radical generation in acute experimental head injury. J. Neurochem. 60, 588-594.
23. Hall, E. D., Andrus, P. K., Yonkers, P. A., Smith, S. L., Zhang, J. R., Taylor, B. M., and Sun, F. F. (1994). Generation and detection of hydroxyl radical following experimental head injury. Ann. NY Acad. Sci. 738, 15-24.
24. Hawthorne, G., Gruen, R. L., and Kaye, A. H. (2009). Traumatic brain injury and long-term quality of life: findings from an Australian study. J. Neurotrauma 26, 1623-1633.
25. Hicdonmez, T., Kanter, M., Tiryaki, M., Parsak, T., and Cobanoglu, S. (2006). Neuroprotective effects of N-acetylcysteine on experimental closed head trauma in rats. Neurochem. Res. 31, 473-481.
26. Jain, K. K. (2008). Neuroprotection in traumatic brain injury. Drug Discov. Today 13, 1082-1089.
27. Jiang, J. Y., Gao, G. Y., Li, W. P., Yu, M. K., and Zhu, C. (2002). Early indicators of prognosis in 846 cases of severe traumatic brain injury. J. Neurotrauma 19, 869-874.
28. Jones, N. C., Cardamone, L., Williams, J. P., Salzberg, M. R., Myers, D., and O'Brien, T. J. (2008). Experimental traumatic brain injury induces a pervasive hyperanxious phenotype in rats. J. Neurotrauma 25, 1367-1374.
29. Jorge, R. E., Acion, L., Starkstein, S. E., and Magnotta, V. (2007). Hippocampal volume and mood disorders after traumatic brain injury. Biol. Psychiatry 62, 332-338.
30. Jorge, R. E., Robinson, R. G., Moser, D., Tateno, A., Crespo-Facorro, B., and Arndt, S. (2004). Major depression following traumatic brain injury. Arch. Gen. Psychiatry 61, 42-50.
31. Jorge, R. E., Robinson, R. G., Starkstein, S. E., and Arndt, S. V. (1993). Depression and anxiety following traumatic brain injury. J. Neuropsychiatry Clin. Neurosci. 5, 369-374.
32. King, N. S. (2003). Post-concussion syndrome: clarity amid the controversy? Br. J. Psychiatry 183, 276-278.
33. Kontos, H. A., and Povlishock, J. T. (1986). Oxygen radicals in brain injury. Cent. Nerv. Syst. Trauma 3, 257-263.
34. Kontos, H. A., and Wei, E. P. (1986). Superoxide production in experimental brain injury. J. Neurosurg. 64, 803-807.
35. Langlois, J. A., Rutland-Brown, W., and Wald, M. M. (2006). The epidemiology and impact of traumatic brain injury: a brief overview. J. Head Trauma Rehabil. 21, 375-378.
36. Li, S., Kuroiwa, T., Katsumata, N., Ishibashi, S., Sun, L. Y., Endo, S., and Ohno, K. (2006). Transient versus prolonged hyperlocomotion following lateral fluid percussion injury in mongolian gerbils. J. Neurosci. Res. 83, 292-300.
37. Lister, R. G. (1987). The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl.) 92, 180-185.
38. Maas, A. I., Stocchetti, N., Bullock, R. (2008). Moderate and severe traumatic brain injury in adults. Lancet Neurol. 7, 728-741.
39. McArthur, R., and Borsini, F. (2006). Animal models of depression in drug discovery: a historical perspective. Pharmacol. Biochem. Behav. 84, 436-452.
40. McIlwain, K. L., Merriweather, M. Y., Yuva-Paylor, L. A., and Paylor, R. (2001). The use of behavioral test batteries: effects of training history. Physiol. Behav. 73, 705-717.
41. Milman, A., Zohar, O., Maayan, R., Weizman, R., and Pick, C. G. (2008). DHEAS repeated treatment improves cognitive and behavioral deficits after mild traumatic brain injury. Eur. Neuropsychopharmacol. 18, 181-187.
42. Morales, D. M., Marklund, N., Lebold, D., Thompson, H. J., Pitkanen, A., Maxwell, W. L., Longhi, L., Laurer, H., Maegele, M., Neugebauer, E., Graham, D. I., Stocchetti, N., and McIntosh, T. K. (2005). Experimental models of traumatic brain injury: do we really need to build a better mousetrap? Neuroscience 136, 971-989.
43. Ohkawa, H., Ohishi, N., and Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95, 351-358.
44. Pandey, D. K., Yadav, S. K., Mahesh, R., and Rajkumar, R. (2009). Depression-like and anxiety-like behavioural aftermaths of impact accelerated traumatic brain injury in rats: a model of comorbid depression and anxiety? Behav. Brain Res. 205, 436-442.
45. Paylor, R., Spencer, C. M., Yuva-Paylor, L. A., and Pieke-Dahl, S. (2006). The use of behavioral test batteries, II: effect of test interval. Physiol. Behav. 87, 95-102.
46. Pelegrin-Valero, C. A., Gomez-Hernandez, R., Munoz-Cespedes, J. M., Fernandez-Guinea, S. D., and Tirapu-Ustarroz, J. (2001). [Nosologic aspects of personality change due to head trauma]. Rev. Neurol. 32, 681-687.
47. Petronilho, F., Feier, G., de Souza, B., Guglielmi, C., Constantino, L. S., Walz, R., Quevedo, J., and Dal-Pizzol, F. (2009). Oxidative stress in brain according to traumatic brain injury intensity. J. Surg. Res., in press.
48. Pick, C. G., Baratz, R., Rubovitch, V., and Frenk, H. (2009). The Influence of alcohol on behavioral recovery following mTBI in mice. J. Neurotrauma, in press.
49. Porsolt, R. D., Bertin, A., and Jalfre, M. (1977). Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther. 229, 327-336.
50. Pullela, R., Raber, J., Pfankuch, T., Ferriero, D. M., Claus, C. P., Koh, S. E., Yamauchi, T., Rola, R., Fike, J. R., and Noble-Haeusslein, L. J. (2006). Traumatic injury to the immature brain results in progressive neuronal loss, hyperactivity and delayed cognitive impairments. Dev. Neurosci. 28, 396-409.
51. Rial, D., Duarte, F. S., Xikota, J. C., Schmitz, A. E., Dafre, A. L., Figueiredo, C. P., Walz, R., and Prediger, R. D. (2009). Cellular prion protein modulates age-related behavioral and neurochemical alterations in mice. Neuroscience 164, 896-907.
52. Sartorius, N., Ustun, T. B., Lecrubier, Y., and Wittchen, H. U. (1996). Depression comorbid with anxiety: results from the WHO study on psychological disorders in primary health care. Br. J. Psychiatry Suppl., 38-43.
53. Scheff, S. W., Baldwin, S. A., Brown, R. W., and Kraemer, P. J. (1997). Morris water maze deficits in rats following traumatic brain injury: lateral controlled cortical impact. J. Neurotrauma 14, 615-627.
54. Schwarzbach, E., Bonislawski, D. P., Xiong, G., and Cohen, A. S. (2006). Mechanisms underlying the inability to induce area CA1 LTP in the mouse after traumatic brain injury. Hippocampus 16, 541-550.
55. Schwarzbold, M., Diaz, A., Martins, E. T., Rufino, A., Amante, L. N., Thais, M. E., Quevedo, J., Hohl, A., Linhares, M. N., and Walz, R. (2008). Psychiatric disorders and traumatic brain injury. Neuropsychiatr. Dis Treat. 4, 797-816.
56. Shapira, M., Licht, A., Milman, A., Pick, C. G., Shohami, E., and Eldar-Finkelman, H. (2007). Role of glycogen synthase kinase-3beta in early depressive behavior induced by mild traumatic brain injury. Mol. Cell Neurosci. 34, 571-577.
57. Smith, S. L., Andrus, P. K., Zhang, J. R., and Hall, E. D. (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.
58. Starkstein, S. E., and Robinson, R. G. (1997). Mechanism of disinhibition after brain lesions. J. Nerv. Ment. Dis. 185, 108-114.
59. Steru, L., Chermat, R., Thierry, B., and Simon, P. (1985). The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology (Berl.) 85, 367-370.
60. Tang, Y. P., Noda, Y., Hasegawa, T., and Nabeshima, T. (1997). A concussive-like brain injury model in mice (I): impairment in learning and memory. J. Neurotrauma 14, 851-862.
61. Taylor, A. N., Rahman, S. U., Tio, D. L., Sanders, M. J., Bando, J. K., Truong, A. H., and Prolo, P. (2006). Lasting neuroendocrineimmune effects of traumatic brain injury in rats. J. Neurotrauma 23, 1802-1813.
62. Tsenter, J., Beni-Adani, L., Assaf, Y., Alexandrovich, A. G., Trembovler, V., and Shohami, E. (2008). Dynamic changes in the recovery after traumatic brain injury in mice: effect of injury severity on T2-weighted MRI abnormalities, and motor and cognitive functions. J. Neurotrauma 25, 324-333.
63. Tsuru-Aoyagi, K., Potts, M. B., Trivedi, A., Pfankuch, T., Raber, J., Wendland, M., Claus, C. P., Koh, S. E., Ferriero, D., and Noble-Haeusslein, L. J. (2009). Glutathione peroxidase activity modulates recovery in the injured immature brain. Ann. Neurol. 65, 540-549.
64. Tweedie, D., Milman, A., Holloway, H. W., Li, Y., Harvey, B. K., Shen, H., Pistell, P. J., Lahiri, D. K., Hoffer, B. J., Wang, Y., Pick, C. G., and Greig, N. H. (2007). Apoptotic and behavioral sequelae of mild brain trauma in mice. J. Neurosci. Res. 85, 805-815.
65. Tyurin, V. A., Tyurina, Y. Y., Borisenko, G. G., Sokolova, T. V., Ritov, V. B., Quinn, P. J., Rose, M., Kochanek, P., Graham, S. H., and Kagan, V. E. (2000). Oxidative stress following traumatic brain injury in rats: quantitation of biomarkers and detection of free radical intermediates. J. Neurochem. 75, 2178-2189.
66. Viggiano, D. (2008). The hyperactive syndrome: metanalysis of genetic alterations, pharmacological treatments and brain lesions which increase locomotor activity. Behav. Brain Res. 194, 1-14.
67. Wang, D., and Corbett, D. (1990). Cerebral ischemia, locomotor activity and spatial mapping. Brain Res. 533, 78-82.
68. Wendel, A. (1981). Glutathione peroxidase. Methods Enzymol. 77, 325-333.
69. Werner, C., and Engelhard, K. (2007). Pathophysiology of traumatic brain injury. Br. J. Anaesth. 99, 4-9.
70. Zohar, O., Schreiber, S., Getslev, V., Schwartz, J. P., Mullins, P. G., and Pick, C. G. (2003). Closed-head minimal traumatic brain injury produces long-term cognitive deficits in mice. Neuroscience 118, 949-955.
71. Zomkowski, A., Oscar Rosa, A., Lin, J., Santos, A. R., Calixto, J. B., and Rodrigues, A. L. S. (2004). Evidence for serotonin receptor subtypes involvement in agmatine antidepressant like-effect in the mouse forced swimming test. Brain Res. 1023, 253-263.