Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015 (2015), Article ID 831490, 15 pages
http://dx.doi.org/10.1155/2015/831490
Research Article

The Roads to Mitochondrial Dysfunction in a Rat Model of Posttraumatic Syringomyelia

1Department of Neurosurgery, Beijing Shijitan Hospital, Capital Medical University, Beijing 100038, China
2Prince of Wales Clinical School, The University of New South Wales, Sydney, NSW 2052, Australia

Received 12 May 2014; Accepted 13 October 2014

Academic Editor: Ancha Baranova

Copyright © 2015 Zhiqiang Hu and Jian Tu. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. A. Backe, R. R. Betz, M. Mesgarzadeh, T. Beck, and M. Clancy, “Post-traumatic spinal cord cysts evaluated by magnetic resonance imaging,” Paraplegia, vol. 29, no. 9, pp. 607–612, 1991. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. A. Biyani and W. S. El Masry, “Post-traumatic syringomyelia: a review of the literature,” Paraplegia, vol. 32, no. 11, pp. 723–731, 1994. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. A. V. Krassioukov, J. C. Furlan, and M. G. Fehlings, “Autonomic dysreflexia in acute spinal cord injury: an under-recognized clinical entity,” Journal of Neurotrauma, vol. 20, no. 8, pp. 707–716, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. G. Wasner, J. Schattschneider, A. Binder, and R. Baron, “Complex regional pain syndrome—diagnostic, mechanisms, CNS involvement and therapy,” Spinal Cord, vol. 41, no. 2, pp. 61–75, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. J. Klekamp, U. Batzdorf, M. Samii, and H. Werner Bothe, “Treatment of syringomyelia associated with arachnoid scarring caused by arachnoiditis or trauma,” Journal of Neurosurgery, vol. 86, no. 2, pp. 233–240, 1997. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. D. Liu, W. Thangnipon, and D. J. McAdoo, “Excitatory amino acids rise to toxic levels upon impact injury to the rat spinal cord,” Brain Research, vol. 547, no. 2, pp. 344–348, 1991. View at Publisher · View at Google Scholar · View at Scopus
  7. S. S. Panter, S. W. Yum, and A. I. Faden, “Alteration in extracellular amino acids after traumatic spinal cord injury,” Annals of Neurology, vol. 27, no. 1, pp. 96–99, 1990. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. R. K. Simpson Jr., C. S. Robertson, and J. C. Goodman, “Spinal cord ischemia-induced elevation of amino acids: extracellular measurement with microdialysis,” Neurochemical Research, vol. 15, no. 6, pp. 635–639, 1990. View at Publisher · View at Google Scholar · View at Scopus
  9. J. J. Lemasters, “V. Necrapoptosis and the mitochondrial permeability transition: shared pathways to necrosis and apoptosis,” The American Journal of Physiology, vol. 276, no. 1, pp. G1–6, 1999. View at Google Scholar · View at Scopus
  10. S. L. Budd and D. G. Nicholls, “Mitochondria in the life and death of neurons,” Essays in Biochemistry, vol. 33, pp. 43–52, 1998. View at Google Scholar · View at Scopus
  11. K. Tsuji, Y. Nakamura, T. Ogata, T. Shibata, and K. Kataoka, “Rapid decrease in ATP content without recovery phase during glutamate-induced cell death in cultured spinal neurons,” Brain Research, vol. 662, no. 1-2, pp. 289–292, 1994. View at Publisher · View at Google Scholar · View at Scopus
  12. A. R. Brodbelt, M. A. Stoodley, A. Watling et al., “The role of excitotoxic injury in post-traumatic syringomyelia,” Journal of Neurotrauma, vol. 20, no. 9, pp. 883–893, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. L. Yang, N. R. Jones, M. A. Stoodley, P. C. Blumbergs, and C. J. Brown, “Excitotoxic model of post-traumatic syringomyelia in the rat,” Spine, vol. 26, no. 17, pp. 1842–1849, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. T. H. Milhorat, R. M. Kotzen, A. L. Capocelli Jr., P. Bolognese, A. A. Bendo, and J. E. Cottrell, “Intraoperative improvement of somatosensory evoked potentials and local spinal cord blood flow in patients with syringomyelia,” Journal of Neurosurgical Anesthesiology, vol. 8, no. 3, pp. 208–215, 1996. View at Publisher · View at Google Scholar · View at Scopus
  15. T. H. Milhorat, A. L. Capocelli Jr., R. M. Kotzen, P. Bolognese, I. M. Heger, and J. E. Cottrell, “Intramedullary pressure in syringomyelia: clinical and pathophysiological correlates of syrinx distension,” Neurosurgery, vol. 41, no. 5, pp. 1102–1110, 1997. View at Publisher · View at Google Scholar · View at Scopus
  16. W. F. Young, R. Tuma, and T. O'Grady, “Intraoperative measurement of spinal cord blood flow in syringomyelia,” Clinical Neurology and Neurosurgery, vol. 102, no. 3, pp. 119–123, 2000. View at Publisher · View at Google Scholar · View at Scopus
  17. National Health and Medical Research Council, Australian Code of Practice for the Care and Use of Animals for Scientific Purposes, National Health and Medical, 7th edition, 2004, http://www.nhmrc.gov.au/_files_nhmrc/publications/attachments/ea16.pdf.
  18. J. Tu, J. Liao, M. A. Stoodley, and A. M. Cunningham, “Differentiation of endogenous progenitors in an animal model of post-traumatic Syringomyelia,” Spine, vol. 35, no. 11, pp. 1116–1121, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. J. Tu, J. Liao, M. A. Stoodley, and A. M. Cunningham, “Reaction of endogenous progenitor cells in a rat model of posttraumatic syringomyelia: laboratory investigation,” Journal of Neurosurgery: Spine, vol. 14, no. 5, pp. 573–582, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. J. Tu, M. A. Stoodley, M. K. Morgan, and K. P. Storer, “Ultrastructure of perinidal capillaries in cerebral arteriovenous malformations,” Neurosurgery, vol. 58, no. 5, pp. 961–969, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. J. Tu, M. A. Stoodley, M. K. Morgan, and K. P. Storer, “Ultrastructural characteristics of hemorrhagic, nonhemorrhagic, and recurrent cavernous malformations,” Journal of Neurosurgery, vol. 103, no. 5, pp. 903–909, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. J. Tu, M. A. Stoodley, M. K. Morgan, and K. P. Storer, “Responses of arteriovenous malformations to radiosurgery: ultrastructural changes,” Neurosurgery, vol. 58, no. 4, pp. 749–758, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. R. Hampp, “Luminometric method,” in Methods of Enzymatic Analysis, H. U. Bergmeyer, Ed., pp. 370–379, Vch Verlagsgesellschaft Mbh, Weinheim, Germany, 1986. View at Google Scholar
  24. J. L. Hintze, “Analysis of variance,” in Number Cruncher Statistical Systems (NCSS) 97-user’s Guide-I, J. L. Hintze, Ed., pp. 205–278, Kaysville, Utah, USA, 1997. View at Google Scholar
  25. P. Bernardi, “Mitochondrial transport of cations: channels, exchangers, and permeability transition,” Physiological Reviews, vol. 79, no. 4, pp. 1127–1155, 1999. View at Google Scholar · View at Scopus
  26. M. Ankarcrona, J. M. Dypbukt, E. Bonfoco et al., “Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function,” Neuron, vol. 15, no. 4, pp. 961–973, 1995. View at Publisher · View at Google Scholar · View at Scopus
  27. R. J. White and I. J. Reynolds, “Mitochondria accumulate Ca2+ following intense glutamate stimulation of cultured rat forebrain neurones,” Journal of Physiology, vol. 498, no. 1, pp. 31–47, 1997. View at Google Scholar · View at Scopus
  28. T.-I. Peng, M.-J. Jou, S.-S. Sheu, and J. T. Greenamyre, “Visualization of NMDA receptor-induced mitochondrial calcium accumulation in striatal neurons,” Experimental Neurology, vol. 149, no. 1, pp. 1–12, 1998. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. K. K. Gunter and T. E. Gunter, “Transport of calcium by mitochondria,” Journal of Bioenergetics and Biomembranes, vol. 26, no. 5, pp. 471–485, 1994. View at Publisher · View at Google Scholar · View at Scopus
  30. M. W. Ward, A. C. Rego, B. G. Frenguelli, and D. G. Nicholls, “Mitochondrial membrane potential and glutamate excitotoxicity in cultured cerebellar granule cells,” Journal of Neuroscience, vol. 20, no. 19, pp. 7208–7219, 2000. View at Google Scholar · View at Scopus
  31. A. C. Rego, M. S. Santos, and C. R. Oliveira, “Glutamate-mediated inhibition of oxidative phosphorylation in cultured retinal cells,” Neurochemistry International, vol. 36, no. 2, pp. 159–166, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. A. K. Stout, H. M. Raphael, B. I. Kanterewicz, E. Klann, and R. Busto, “Glutamate-induced neuron death requires mitochondrial calcium uptake,” Nature Neuroscience, vol. 1, no. 5, pp. 366–373, 1998. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. S. Y. Seo, E. Y. Kim, H. Kim, and B. J. Gwag, “Neuroprotective effect of high glucose against NMDA, free radical, and oxygen-glucose deprivation through enhanced mitochondrial potentials,” Journal of Neuroscience, vol. 19, no. 20, pp. 8849–8855, 1999. View at Google Scholar · View at Scopus
  34. R. D. Randall and S. A. Thayer, “Glutamate-induced intracellular acidification of cultured hippocampal neurons demonstrates altered energy metabolism resulting from Ca2+ loads,” Journal of Neurophysiology, vol. 72, no. 6, pp. 2563–2569, 1994. View at Google Scholar · View at Scopus
  35. B. Khodorov, V. Pinelis, O. Vergun, T. Storozhevykh, and N. Vinskaya, “Mitochondrial deenergization underlies neuronal calcium overload following a prolonged glutamate challenge,” FEBS Letters, vol. 397, no. 2-3, pp. 230–234, 1996. View at Publisher · View at Google Scholar · View at Scopus
  36. J. M. Dubinsky and Y. Levi, “Calcium-induced activation of the mitochondrial permeability transition in hippocampal neurons,” Journal of Neuroscience Research, vol. 53, pp. 728–741, 1998. View at Google Scholar
  37. K. Hasegawa, H. Yoshioka, T. Sawada, and H. Nishikawa, “Direct measurement of free radicals in the neonatal mouse brain subjected to hypoxia: an electron spin resonance spectroscopic study,” Brain Research, vol. 607, no. 1-2, pp. 161–166, 1993. View at Publisher · View at Google Scholar · View at Scopus
  38. W. Cao, J. M. Carney, A. Duchon, R. A. Floyd, and M. Chevion, “Oxygen free radical involvement in ischemia and reperfusion injury to brain,” Neuroscience Letters, vol. 88, no. 2, pp. 233–238, 1988. View at Publisher · View at Google Scholar · View at Scopus
  39. J. A. Dykens, “Isolated cerebral and cerebellar mitochondria produce free radicals when exposed to elevated Ca2+ and Na+: Implications for neurodegeneration,” Journal of Neurochemistry, vol. 63, no. 2, pp. 584–591, 1994. View at Google Scholar · View at Scopus
  40. L. L. Dugan, S. L. Sensi, L. M. T. Canzoniero et al., “Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate,” Journal of Neuroscience, vol. 15, no. 10, pp. 6377–6388, 1995. View at Google Scholar · View at Scopus
  41. C. Giulivi, A. Boveris, and E. Cadenas, “Hydroxyl radical generation during mitochondrial electron transfer and the formation of 8-hydroxydesoxyguanosine in mitochondrial DNA,” Archives of Biochemistry and Biophysics, vol. 316, no. 2, pp. 909–916, 1995. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. C. A. Piantadosi and J. Zhang, “Mitochondrial generation of reactive oxygen species after brain ischemia in the rat,” Stroke, vol. 27, no. 2, pp. 327–332, 1996. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Zhang, O. Marcillat, C. Giulivi, L. Ernster, and K. J. A. Davies, “The oxidative inactivation of mitochondrial electron transport chain components and ATPase,” The Journal of Biological Chemistry, vol. 265, no. 27, pp. 16330–16336, 1990. View at Google Scholar · View at Scopus
  44. R. Radi, S. Sims, A. Cassina, and J. F. Turrens, “Roles of catalase and cytochrome C in hydroperoxide-dependent lipid peroxidation and chemiluminescence in rat heart and kidney mitochondria,” Free Radical Biology and Medicine, vol. 15, no. 6, pp. 653–659, 1993. View at Publisher · View at Google Scholar · View at Scopus
  45. K. M. A. Welch, L. R. Caplan, D. J. Reis, S. K. Siesjo, and B. Weir, Primer on Cerebrovascular Diseases, Academic Press, San Diego, Calif, USA, 1997.
  46. B. K. Siesjö, K. I. Katsura, T. Kristián, P.-A. Li, and P. Siesjö, “Molecular mechanisms of acidosis-mediated damage,” Acta Neurochirurgica, Supplement, vol. 1996, no. 66, pp. 8–14, 1996. View at Google Scholar · View at Scopus
  47. I. J. Furlong, R. Ascaso, A. Lopez Rivas, and M. K. L. Collins, “Intracellular acidification induces apoptosis by stimulating ICE-like protease activity,” Journal of Cell Science, vol. 110, no. 5, pp. 653–661, 1997. View at Google Scholar · View at Scopus
  48. S. Matsuyama, J. Llopis, Q. L. Deveraux, R. Y. Tsien, and J. C. Reed, “Changes in intramitochondrial and cytosolic pH: early events that modulate caspase activation during apoptosis,” Nature Cell Biology, vol. 2, no. 6, pp. 318–325, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  49. W. C. Earnshaw, L. M. Martins, and S. H. Kaufmann, “Mammalian caspases: structure, activation, substrates, and functions during apoptosis,” Annual Review of Biochemistry, vol. 68, pp. 383–424, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. D. Ding, S. I. Moskowitz, R. Li et al., “Acidosis induces necrosis and apoptosis of cultured hippocampal neurons,” Experimental Neurology, vol. 162, no. 1, pp. 1–12, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  51. C. A. Giller and S. S. Finn, “Intraoperative measurement of spinal cord blood velocity using pulsed doppler ultrasound. A case report,” Surgical Neurology, vol. 32, no. 5, pp. 387–393, 1989. View at Publisher · View at Google Scholar · View at Scopus
  52. L. R. Caplan, A. B. Norohna, and L. L. Amico, “Syringomyelia and arachnoiditis,” Journal of Neurology Neurosurgery and Psychiatry, vol. 53, no. 2, pp. 106–113, 1990. View at Publisher · View at Google Scholar · View at Scopus
  53. G. Guizar-Sahagun, I. Grijalva, I. Madrazo et al., “Development of post-traumatic cysts in the spinal cord of rats subjected to severe spinal cord contusion,” Surgical Neurology, vol. 41, no. 3, pp. 241–249, 1994. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Ohashi, T. Morimoto, K. Kawata, T. Yamada, and T. Sakaki, “Correlation between spinal cord blood flow and arterial diameter following acute spinal cord injury in rats,” Acta Neurochirurgica, vol. 138, no. 3, pp. 322–329, 1996. View at Publisher · View at Google Scholar · View at Scopus
  55. H. S. Sharma, Y. Olsson, F. Nyberg, and P. K. Dey, “Prostaglandins modulate alterations of microvascular permeability, blood flow, edema and serotonin levels following spinal cord injury: an experimental study in the rat,” Neuroscience, vol. 57, no. 2, pp. 443–449, 1993. View at Publisher · View at Google Scholar · View at Scopus
  56. C. H. Tator and M. G. Fehlings, “Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms,” Journal of Neurosurgery, vol. 75, no. 1, pp. 15–26, 1991. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. H. Westergren, M. Farooque, Y. Olsson, and A. Holtz, “Spinal cord blood flow changes following systemic hypothermia and spinal cord compression injury: an experimental study in the rat using Laser-Doppler flowmetry,” Spinal Cord, vol. 39, no. 2, pp. 74–84, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. I. R. Rise, C. Risöe, and O. J. Kirkeby, “Cerebrovascular effects of high intracranial pressure after moderate hemorrhage,” Journal of Neurosurgical Anesthesiology, vol. 10, no. 4, pp. 224–230, 1998. View at Publisher · View at Google Scholar · View at Scopus
  59. W. F. Young, R. H. Rosenwasser, U. S. Vasthare, and R. F. Tuma, “Preservation of post-compression spinal cord function by infusion of hypertonic saline,” Journal of Neurosurgical Anesthesiology, vol. 6, no. 2, pp. 122–127, 1994. View at Publisher · View at Google Scholar · View at Scopus
  60. B. E. Levin, V. H. Routh, L. Kang, N. M. Sanders, and A. A. Dunn-Meynell, “Neuronal glucosensing: what do we know after 50 years?” Diabetes, vol. 53, no. 10, pp. 2521–2528, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. W. S. Da-Silva, A. Gómez-Puyou, M. T. de Gómez-Puyou et al., “Mitochondrial bound hexokinase activity as a preventive antioxidant defense. Steady-state ADP formation as a regulatory mechanism of membrane potential and reactive oxygen species generation in mitochondria,” The Journal of Biological Chemistry, vol. 279, no. 38, pp. 39846–39855, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. L. Kang, A. A. Dunn-Meynell, V. H. Routh et al., “Glucokinase is a critical regulator of ventromedial hypothalamic neuronal glucosensing,” Diabetes, vol. 55, no. 2, pp. 412–420, 2006. View at Google Scholar · View at Scopus
  63. A. Tabernero, J. M. Medina, and C. Giaume, “Glucose metabolism and proliferation in glia: role of astrocytic gap junctions,” Journal of Neurochemistry, vol. 99, no. 4, pp. 1049–1061, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. G. Majno and I. Joris, “Apoptosis, oncosis, and necrosis: an overview of cell death,” The American Journal of Pathology, vol. 146, no. 1, pp. 3–15, 1995. View at Google Scholar · View at Scopus
  65. I. Szabo and M. Zoratti, “The giant channel of the inner mitochondrial membrane is inhibited by cyclosporin A,” The Journal of Biological Chemistry, vol. 266, no. 6, pp. 3376–3379, 1991. View at Google Scholar · View at Scopus