Cellular alterations in human traumatic brain injury: Changes in mitochondrial morphology reflect regional levels of injury severity

Journal of Neurotrauma

Volumn 30, Issue 5, 2013, Pages 367-381

  Balan, Irina S ^a   Saladino, Andrew J ^a,b   Aarabi, Bizhan ^a   Castellani, Rudolf J ^a   Wade, Christine ^a   Stein, Deborah M ^a   Eisenberg, Howard M ^a   Chen, Hegang H ^a   Fiskum, Gary ^a  

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

^b BALTIMORE VA MEDICAL CENTER   (United States)

Author keywords

cristae; electron microscopy; matrix; penumbra

Indexed keywords

ADOLESCENT; ADULT; AGED; ARTICLE; BRAIN CORTEX; BRAIN MITOCHONDRION; BRAIN SURGERY; CELL ORGANELLE; CELL ULTRASTRUCTURE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOARCHITECTURE; ELECTRON MICROSCOPY; EPILEPSY; FEMALE; HUMAN; HUMAN TISSUE; INJURY SEVERITY; MALE; NERVE CELL DEGENERATION; PHENOTYPE; QUANTITATIVE ANALYSIS; TRAUMATIC BRAIN INJURY;

ADOLESCENT; ADULT; AGED; BRAIN; BRAIN INJURIES; FEMALE; HUMANS; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MIDDLE AGED; MITOCHONDRIA; YOUNG ADULT;

EID: 84874697045     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2339     Document Type: Article

References (66)

1. Fiskum, G. (2000). Mitochondrial participation in ischemic and traumatic neural cell death. J. Neurotrauma 17, 843-855.
2. Lifshitz, J., Sullivan, P.G., Hovda, D.A., Wieloch, T., and McIntosh, T.K. (2004). Mitochondrial damage and dysfunction in traumatic brain injury. Mitochondrion 4, 705-713.
3. Okonkwo, D.O., and Povlishock, J.T. (1999). An intrathecal bolus of cyclosporin A before injury preserves mitochondrial integrity and attenuates axonal disruption in traumatic brain injury. J. Cereb. Blood Flow Metab. 19, 443-451.
4. Bereiter-Hahn, J., and Jendrach, M. (2010). Mitochondrial dynamics. Int. Rev. Cell Mol. Biol. 284, 1-65.
5. Garrido, N., Griparic, L., Jokitalo, E., Wartiovaara, J., van der Bliek, A.M., and Spelbrink, J.N. (2003). Composition and dynamics of human mitochondrial nucleoids. Mol. Biol. Cell. 14, 1583-1596.
6. Liu, X., and Hajnoczky, G. (2011). Altered fusion dynamics underlie unique morphological changes in mitochondria during hypoxia-reoxygenation stress. Cell Death Differ. 18, 1561-1572.
7. Lyamzaev, K.G., Nepryakhina, O.K., Saprunova, V.B., Bakeeva, L.E., Pletjushkina, O.Y., Chernyak, B.V., and Skulachev, V.P. (2008). Novel mechanism of elimination of malfunctioning mitochondria (mitoptosis): formation of mitoptotic bodies and extrusion of mitochondrial material from the cell. Biochim. Biophys. Acta 1777, 817-825.
8. Mannella, C.A. (2006). The relevance of mitochondrial membrane topology to mitochondrial function. Biochim. Biophys. Acta 1762, 140-147.
9. Zick, M., Rabl, R., and Reichert, A.S. (2009). Cristae formationlinking ultrastructure and function of mitochondria. Biochim. Biophys. Acta 1793, 5-19.
10. Jahani-Asl, A., Pilon-Larose, K., Xu, W., MacLaurin, J.G., Park, D.S., McBride, H.M., and Slack, R.S. (2011). The mitochondrial inner membrane GTPase, optic atrophy 1 (Opa1), restores mitochondrial morphology and promotes neuronal survival following excitotoxicity. J. Biol. Chem. 286, 4772-4782.
11. Chen, H., and Chan, D.C. (2009). Mitochondrial dynamics - fusion, fission, movement, and mitophagy - in neurodegenerative diseases. Hum. Mol. Genet. 18, R169-R176.
12. Gunawardena, S., and Goldstein, L.S. (2004). Cargo-carrying motor vehicles on the neuronal highway: transport pathways and neurodegenerative disease. J. Neurobiol. 58, 258-271.
13. Liesa, M., Palacin, M., and Zorzano, A. (2009). Mitochondrial dynamics in mammalian health and disease. Physiol. Rev. 89, 799-845.
14. Morganti-Kossmann, M.C., Yan, E., and Bye, N. (2010). Animal models of traumatic brain injury: is there an optimal model to reproduce human brain injury in the laboratory? Injury 41, Suppl 1, S10-S13.
15. Vink, R., and Nimmo, A.J. (2009). Multifunctional drugs for head injury. Neurotherapeutics 6, 28-42.
16. Castejon, O.J., and De Castejon, H.V. (2004). Structural patterns of injured mitochondria in human oedematous
17. Balan, I.S., Kristian, T., Liu, C., Saladino, A.J., and Hu, B. (2012). Morphological assessments of global cerebral ischemia: Electron microscopy, in: Animal Models of Acute Neurological Injuries II. J. Chen, X.-M. Xu, Z.C. Xu, and J.H. Zhang (eds). Humana Press: New York, pps. 29-46.
18. Cragg, B.G. (1976) Ultrastructural features of human cerebral cortex. J. Anat. 121, 331-362.
19. Harris, K.M. (2008). Diversity in synapse structure and composition, in: Structural and Functional Organization of the Synapse. J.W. Hell, and M.D. Ehlers (eds). Springer: New York, pps. 1-21.
20. Mishchenko, Y., Hu, T., Spacek, J., Mendenhall, J., Harris, K.M., and Chklovskii, D.B. (2010) Ultrastructural analysis of hippocampal neuropil from the connectomics perspective. Neuron 67, 1009-1020.
21. Ong, W.Y., and Garey, L.J. (1991). Ultrastructural characteristics of human adult and infant cerebral cortical neurons. J. Anat. 175, 79- 104.
22. Peters A., Palay S.L., and Webster, H. deF (1991). The Fine Structure of the Nervous System. Oxford University Press: New York.
23. Balan, I.S., Fiskum, G., and Kristian, T. (2010). Visualization and quantification of NAD(H) in brain sections by a novel histo-enzymatic nitrotetrazolium blue staining technique. Brain Res. 1316, 112-119.
24. Barsoum, M.J., Yuan, H., Gerencser, A.A., Liot, G., Kushnareva, Y., Gra?ber, S., Kovacs, I., Lee, W.D., Waggoner, J., Cui, J., White, A.D., Bossy, B., Martinou, J.C., Youle, R.J., Lipton, S.A., Ellisman, M.H., Perkins, G.A., and Bossy-Wetzel, E. (2006). Nitric oxide-induced mitochondrial fission is regulated by dynamin-related GTPases in neurons. EMBO J. 25, 3900-3911.
25. Benani, A., Barquissau, V., Carneiro, L., Salin, B., Colombani, A.L., Leloup, C., Casteilla, L., Rigoulet, M., and Penicaud, L. (2009). Method for functional study of mitochondria in rat hypothalamus. J. Neurosci. Methods 178, 301-307.
26. Hackenbrock, C.R. (1966). Ultrastructural bases for metabolically linked mechanical activity in mitochondria. I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria. J. Cell Biol. 30, 269-297.
27. Hackenbrock, C.R. (1968). Ultrastructural bases for metabolically linked mechanical activity in mitochondria. II. Electron transportlinked ultrastructural transformations in mitochondria. J. Cell Biol. 37, 345-369.
28. Hackenbrock, C.R., Rehn, T.G., Weinbach, E.C., and Lemasters, J.J. (1971). Oxidative phosphorylation and ultrastructural transformation in mitochondria in the intact ascites tumor cell. J. Cell Biol. 51, 123-137.
29. Lai, Y., Chen, Y., Watkins, S.C., Nathaniel, P.D., Guo, F., Kochanek, P.M., Jenkins, L.W., Szabó, C., and Clark, R.S. (2008). Identification of poly-ADP-ribosylated mitochondrial proteins after traumatic brain injury. J. Neurochem. 104, 1700-1711.
30. Singh, I.N., Sullivan, P.G., Deng, Y., Mbye, L.H., and Hall, E.D. (2006). Time course of post-traumatic mitochondrial oxidative damage and dysfunction in a mouse model of focal traumatic brain injury: implications for neuroprotective therapy. J. Cereb. Blood Flow Metab. 26, 1407-1418.
31. Sloper, J.J., Hiorns, R.W., and Powell, T.P. (1979). A qualitative and quantitative electron microscopic study of the neurons in the primate motor and somatic sensory cortices. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 285, 141-171.
32. Packer, L. (1970). Relation of structure to energy coupling in rat liver mitochondria. Fed. Proc. 29, 1533-1540.
33. Skulachev, V.P., Bakeeva, L.E., Chernyak, B.V., Domnina, L.V., Minin, A.A., Pletjushkina, O.Y., Saprunova, V.B., Skulachev, I.V., Tsyplenkova, V.G., Vasiliev, J.M., Yaguzhinsky, L.S., and Zorov, D.B. (2004). Thread-grain transition of mitochondrial reticulum as a step of mitoptosis and apoptosis. Mol. Cell Biochem. 256-257, 341-358.
34. Neuspiel, M., Schauss, A.C., Braschi, E., Zunino, R., Rippstein, P., Rachubinski, R.A., Andrade-Navarro, M.A., and McBride, H.M. (2008). Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr. Biol. 18, 102-108.
35. Greenawalt, J.W., Rossi, C.S., and Lehninger, A.L. (1964). Effect of active accumulation of calcium and phosphate ions on the structure of rat liver mitochondria. J. Cell Biol. 23, 21-38.
36. Trump, B.F., Mergner, W.J., Kahng, M.W., and Salandino, A.J. (1976). Studies on the subcellular pathophysiology of ischemia. Circulation 53, Suppl 3, I17-I26.
37. Liu, C., Gao, Y., Barrett, J., and Hu, B. (2010). Autophagy and protein aggregation after brain ischemia. J. Neurochem. 115, 68-78.
38. Myron, D.R., and Connelly, J.L. (1971). The morphology of the swelling process in rat liver mitochondria. J. Cell Biol. 48, 291- 302.
39. Popov, V., Medvedev, N.I., Davies, H.A., and Stewart, M.G. (2005). Mitochondria form a filamentous reticular network in hippocampal dendrites but are present as discrete bodies in axons: a three-dimensional ultrastructural study. J. Comp. Neurol. 492, 50-65.
40. Trump, B.F., Goldblatt, P.J., and Stowell, R.E. (1965). Studies on necrosis of mouse liver in vitro. Ultrastructural alterations in the mitochondria of hepatic parenchymal cells. Lab. Invest. 14, 343-371.
41. Johannessen, J.V. (1978). Electron Microscopy in Human Medicine: Instrumentation and techniques. J.V. Johannessen (ed). McGraw-Hill: New York, pps. 1-348.
42. Sanchez, V., Feinstein, S.D., Lunardi, N., Joksovic, P.M., Boscolo, A., Todorovic, S.M, and Jevtovic-Todorovic, V. (2011) General anesthesia causes long-term impairment of mitochondrial morphogenesis and synaptic transmission in developing rat brain. Anesthesiology 115, 992-1002.
43. Immonen, R., Heikkinen, T., Ta?htivaara, L., Nurmi, A., Stenius, T.K., Puoliva?li, J., Tuinstra, T., Phinney, A.L., Van Vliet, B., Yrja?nheikki, J., and Gro?hn, O. (2010). Cerebral blood volume alterations in the perilesional areas in the rat brain after traumatic brain injury - comparison with behavioral outcome. J. Cereb. Blood Flow Metab. 30, 1318-1328.
44. Taiushev, K.G., and Shustova, T.I. (1999). [Histologic foundations for evaluation of the crushed wound of the cerebrum in the clinical course of cranio-cerebral trauma as an intracranial extensive process]. (Rus) Morfologiia 116, 7-11.
45. Taiushev, K.G., Zotov, IuV., Kaganovskaia, E.A., Kasumov, R.D., and Shustova, T.I. (1990). [Changes in human cerebral cortex in various areas of concussion in severe cranio-cerebral injury.] (Rus) Arkh. Anat. Gistol. Embriol. 99, 26-33.
46. Thomale, U.W., Griebenow, M., Mautes, A., Beyer, T.F., Dohse, N.K., Stroop, R., Sakowitz, O.W., Unterberg, A.W., and Stover, J.F. (2007). Heterogeneous regional and temporal energetic impairment following controlled cortical impact injury in rats. Neurol. Res. 29, 594-603.
47. Ugriumov, V.M., Zotov, IuV., Tigliev, G.S., and Kondakov, E.N. (1977). [Several pathophysiologic grounds for radical removal of contusion foci from the cerebral hemispheres]. (Rus) Zh. Vopr. Neirokhir. Im. N. N. Burdenko, 3-7.
48. Yin, W., Signore, A.P., Iwai, M., Cao, G., Gao, Y., and Chen, J. (2008). Rapidly increased neuronal mitochondrial biogenesis after hypoxic-ischemic brain injury. Stroke 39, 3057-3063.
49. Frank, S., Gaume, B., Bergmann-Leitner, E.S., Leitner, W.W., Robert, E.G., Catez, F., Smith, C.L., and Youle, R.J. (2001). The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1, 515-525.
50. 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.
51. Colbourne, F., Sutherland, G.R., and Auer, R.N. (1999). Electron microscopic evidence against apoptosis as the mechanism of neuronal death in global ischemia. J. Neurosci. 19, 4200-4210.
52. Solenski, N.J., diPierro, C.G., Trimmer, P.A., Kwan, A.L., and Helms, G.A. (2002). Ultrastructural changes of neuronal mitochondria after transient and permanent cerebral ischemia. Stroke 33, 816-824.
53. Ahn, E.S., Robertson, C.L., Vereczki, V., Hoffman, G.E., and Fiskum, G. (2008). Normoxic ventilatory resuscitation following controlled cortical impact reduces peroxynitrite-mediated protein nitration in the hippocampus. J. Neurosurg. 108, 124-131.
54. Kristian, T., and Siesjo?, B.K. (1996). Calcium-related damage in ischemia. Life Sci. 59, 357-367.
55. Lifshitz, J., Friberg, H., Neumar, R.W., Raghupathi, R., Welsh, F.A., Janmey, P., Saatman, K.E., Wieloch, T., Grady, M.S., and McIntosh, T.K. (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.
56. Starkov, A.A., Chinopoulos, C., and Fiskum, G. (2004). Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 36, 257-264.
57. Bu? ki, 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.
58. Kroemer, G., and Reed, J.C. (2000). Mitochondrial control of cell death. Nat. Med. 6, 513-519.
59. Mazzeo, A.T., Beat, A., Singh, A., and Bullock, M.R. (2009). The role of mitochondrial transition pore, and its modulation, in traumatic brain injury and delayed neurodegeneration after TBI. Exp. Neurol. 218, 363-370.
60. Sullivan, P.G., Rabchevsky, A.G., Waldmeier, P.C., and Springer, J.E. (2005). Mitochondrial permeability transition in CNS trauma: cause or effect of neuronal cell death? J. Neurosci. Res. 79, 231-239.
61. Bu ki, A., Okonkwo, D.O., and Povlishock, J.T. (1999). Postinjury cyclosporin A administration limits axonal damage and disconnection in traumatic brain injury. J. Neurotrauma 16, 511-521.
62. Cook, A.M., Whitlow, J., Hatton, J., and Young, B. (2009). Cyclosporine A for neuroprotection: establishing dosing guidelines for safe and effective use. Expert Opin. Drug Saf. 8, 411-419.
63. Sullivan, P.G., Sebastian, A.H., and Hall, E.D. (2011). Therapeutic window analysis of the neuroprotective effects of cyclosporine A after traumatic brain injury. J. Neurotrauma 28, 311-318.
64. Hatton, J., Rosbolt, B., Empey, P., Kryscio, R., and Young, B. (2008). Dosing and safety of cyclosporine in patients with severe brain injury. J. Neurosurg. 109, 699-707.
65. Mazzeo, A.T., Brophy, G.M., Gilman, C.B., Alves, O.L., Robles, J.R., Hayes, R.L., Povlishock, J.T., and Bullock, M.R. (2009). Safety and tolerability of cyclosporin a in severe traumatic brain injury patients: results from a prospective randomized trial. J. Neurotrauma 26, 2195-2206.
66. Perez-Pinzon, M.A., Stetler, R.A., and Fiskum, G. (2012). Novel mitochondrial targets for neuroprotection. J. Cereb. Blood Flow Metab. 32, 1362-1376.