Early administration of methylprednisolone decreases apoptotic cell death after spinal cord injury

Histology and Histopathology

Volumn 21, Issue 10-12, 2006, Pages 1091-1102

  Vaquero, Jesús ^a,b   Zurita, M ^a   Oya, S ^a   Aguayo, C ^a   Bonilla, C ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Apoptosis; F7 26 marker; Methylprednisolone; Spinal cord injury

Indexed keywords

DNA FRAGMENT; GLIAL FIBRILLARY ACIDIC PROTEIN; METHYLPREDNISOLONE; MONOCLONAL ANTIBODY; SINGLE STRANDED DNA; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY WEIGHT; BOLUS INJECTION; CELL COUNT; CELL DEATH; CONTROLLED STUDY; CONTUSION; ELECTRON MICROSCOPY; EXPERIMENTAL MODEL; FEMALE; GLIA CELL; IMMUNOHISTOCHEMISTRY; NERVE CELL; NONHUMAN; PARAPLEGIA; PROTEIN EXPRESSION; RAT; SINGLE DRUG DOSE; SPINAL CORD INJURY; TIME; TREATMENT OUTCOME; ANIMAL; GLIA; METABOLISM; METHODOLOGY; PATHOLOGY; SPINAL CORD; WISTAR RAT;

ANIMALIA; RATTUS NORVEGICUS;

ANIMALS; APOPTOSIS; BODY WEIGHT; CELL DEATH; FEMALE; IMMUNOHISTOCHEMISTRY; METHYLPREDNISOLONE; MICROSCOPY, ELECTRON; NEUROGLIA; NEURONS; NEUROPROTECTIVE AGENTS; RATS; RATS, WISTAR; SPINAL CORD; SPINAL CORD INJURIES; TIME FACTORS;

EID: 33746759560     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (93)

1. Allen A.R. (1914). Remarks on the histopathological changes in the spinal cord due to impact. An experimental study. J. Nerv. Ment. Dis. 41, 141-147.
2. Anderson D.K., Saunders R.D., Demediuk P., Dugan L.L., Braughler J.M., Hall E.D., Means E.D. and Horrocks L.A. (1985). Lipid hydrolisis and peroxidation in injured spinal cord: partial protection with methylprednisolone or vitamin E and selenium. Cent. Nerv. Syst. Trauma 2, 257-267.
3. Bartholdl D. and Schwab M. E. (1995). Methylprednisolone inhibits early inflamatory processes but no ischemic cell death after experimental spinal cord lesion in the rat. Brain Res. 672, 177-186.
4. Beato M. (1989). Gene regulation by steroids hormones. Cell 56, 335-344,
5. Beattie M.S., Farooqui A.A. and Bresnahan J.C. (2000). Review of current evidence for apoptosis after spinal cord injury. J. Neurotrauma 17, 915-925.
6. Behrmann D.L., Bresnahan J.C. and Beattie M.S. (1994). Modeling of acute spinal cord injury in the rat: neuroprotection and enhanced recovery with methylprednisolone, U-74006F and YM-14673. Exp. Neurol. 126, 61-75.
7. Beks J.W.F., Doorenbos H. and Walstra G.J.M. (1972). Clinical experiences with steroids in neurosurgical patients. In: Steroids and brain edema. Reulen H.J. and Schürmann K. (eds). Berlin. Heidelberg. New York. Springer-Verlag. pp 233-238.
8. Benton R.L., Ross C.D. and Miller K.E. (2001). Spinal taurine levels are increased 7 and 30 days following methylprednisolone treatment of spinal cord injury in rats. Brain Res. 893, 292-300.
9. Bracken M.B. (1991). Treatment of acute spinal cord injury with methylprednisolone: results of a multicenter, randomized clinical trial. J. Neurotrauma 8 (Suppl 1), S47-S52.
10. Bracken M.B., Aldrich E.F., Herr D.L., Hitchon P.W,, Holford T.R., Marshall L.F., Nockels R.P., Pascale M.B., Shepard M.J., Sonntag V.K., Winn H.R. and Young W. (2000). Clinical measurement statistical analysis, and risk-benefit: controversies from trials of spinal injury. J. Trauma 48, 558-561.
11. Bracken M.B., Shepard M.J., Collins W.F., Holford T.R., Baskin D.S., Eisenberg H.M., Flamm E., Leo-Summers L., Maroon J., Marshall L.F., Perot P.L., Piepmeier J., Sonntag V.K.H., Wagner F.C., Wilberger J.E., Winn H.R. and Young W. (11992). Methylprednisolone or naloxone treatment after cute spinal cord injury: 1-year follow-up data. J. Neurosurg. 76, 23-31.
12. Bracken M.B., Shepard M.J., Collins W.F., Holford T.R., Young W., Baskin D.S., Eisenberg H.M., Flamm E., Leo-Summers L, Maroon J., Marshall L.F., Perot P.L. jr., Piepmeier J., Sonntag V.K.H., Wagner F.C., Wlberger J.E. and Winn H.R. (1990). A randomized, controlled trial of methylprednisolone or naloxone in the treatment of acute spinal cord injury. Results of the second National Acute Spinal Cord Injury Study. N. Engl. J. Med. 322, 1405-1411.
13. Brandoli C., Shl B., Pflug B., Andrew, P., Wrathall J.R. and Mochetti I. (2001). Dexamethasone reduces the expression of p75 neurotrophin receptor and apoptosis in contused spinal cord. Brain Res. Mol. Brain Res. 87, 61-70.
14. Braughler J.M. and Hall E.D. (1989). Central nervous system trauma and stroke. I. Biochemical considerations for oxygen radical formation and lipid peroxidation. Free Radic. Biol. Med. 6, 289-301.
15. Brune B., Von-Knthen A. and Sandau K.B. (1998). Nitric oxide and its role in apoptosis. Eur. J. Pharmacol. 351, 261-272.
16. Clark R.S., Kochanek P.M., Chen M., Watkins S.C., Marion D.W., Chen J., Hamilton R.L., Loeffert J.E. and Graham S.H. (1999). Increases in BcI-2 and cleavage of caspase-1 and caspase-3 in human brain after head injury. FASEB J. 13, 813-821.
17. Constantini S. and Young W. (1994). The effects of methylprednisolone and the ganglioside GM1 on acute spinal cord injury in rats. J. Neurosurg. 80, 97-111.
18. Crowe M.J., Shumannn S.L., Masters J.N., Bresnahan J.C. and Beattie M.S. (1995). Morphological evidence suggesting apoptotic nuclei in spinal cord injury. Soc. Neurosci. Abstr. 21, 232.
19. Crowe M.J., Bresnahan J.C., Shuman S.L., Masters J.N. and Beattie M.S. (1997). Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat. Med. 3, 73-76.
20. Cummings M.C., Winterford C.M. and Walker N.I. (1997). Apoptosis. Am. J. Surg. Pathol. 21, 88-101.
21. Chen A., Xu X.M., Kleitman N. and Bunge B. (1996). Mehtylprednisolone administration improves axonal regeneration into schwann cell grafts in transected adult rat thoracic spinal cord. Exp. Neurol. 138, 261-276.
22. Chen T.C., Mackic J.B., Mc Comb J.G., Gianotta S.L., Weiss M.H. and Zlokovic B.V. (1996). Cellular uptake and transport of methylprednisolone at the blood-brain barrier. Neurosurgery 38, 348-354.
23. Chomcynski P., Mackey K., Drews R. and Wilfinger W. (1997). DNAzol: a reagent for the rapid isolation of genomic DNA. BioTechniques 22, 550-553.
24. Demopoulos H.B., Milvy P., Kakari S. and Ransohoff J. (1973). Molecular aspects of membrane structure in cerebral edema. In: Steroids and brain edema. Reulen J.H. and Schuermann K. (eds). Springer. New York. pp 29-39.
25. Demopoulos H.B., Flamm E.S., Seligman M.L., Pietronigro D.D., Tomasula J. and Decrescito V. (1982). Further studies on free-radical pathology in the major central nervous system disorders: effects of very high doses of methylprednisolone on the functional outcome, morphology and chemistry of experimental spinal cord impact injury. Can. J. Physiol. Pharmacol. 60, 1415-1424.
26. Dohrmann G.J., Wick K.M. and Bucy P.C. (11973). Spinal cord blood flow patterns in experimental traumatic paraplegia. J. Neurosurg. 38, 52-58.
27. Emery E., Aldana P., Bunge M.B., Puckett W., Srinivasan A., Keane R.W., Bethea J. and Levi A.D. (1998). Apoptosis after traumatic human spinal cord. J. Neurosurg. 89, 911-920.
28. Faden A.I., Jacobs T.P., Patrick D.H. and Smith M.T. (1984). Megadose corticosteriod therapy following experimental traumatic spinal cord injury. J. Neurosurg. 60, 712-717.
29. Faden A.I., Jacobs T.P., Smith M.T. and Holaday J.W. (1983). Comparasion of thyrotropin-releasing hormone (TRH), naloxone and dexamethasone treatment in experimental spinal injuries. Neurology 33, 673-678.
30. Ferlini C., Kunkl A., Scambia, G. and Fattorossi A. (1997). The use of apostain in identifying early apoptosis. J. Immunol. Methods 205, 95-101.
31. Frankfurt O.S., Robb J.A., Sugarbaker E.V. and Villa L. (1996). Monoclonal antibody to single-stranded DNA is a specific and sensitive cellular marker of apoptosis. Exp. Cell Res. 226, 387-397.
32. Galicich J.H. and French L.A. (1961). Use of dexamethasone in treatment of cerebral edema associated with brain tumors. Lancet 81, 46-53.
33. Green B.A. and Wagner F.C. (1973). Evolution of edema in the acutely injured spinal cord: a fluorescent microscopic study. Surg. Neurol. 1, 98-101.
34. Green B.A., Kahn T. and Klose K.J. (1980). A comparative study of steroid therapy in acute experimental spinal cord injury. Surg. Neurol. 13, 91-97.
35. Hall E.D. (1992). The neuroprotective pharmacology of methylprednisolone. J. Neurosurg. 76,13-22.
36. Hall E.D. and Braughler J.M. (1993). Free radicals in CNS injury. Res. Publ. Assoc. Res. Nerv. Ment. Dis. 71, 81-105.
37. Hall E.D. and Braughler J.M. (1982). Glucocorticoid mechanims in acute spinal cord injury: a review and therapeutic rationale. Surg. Neurol. 18, 320-327.
38. Hall E.D., Daniel L.W. and Braughler J.M. (1984). Effects of a single large dose of methylprednisolone sodium succinate on experimental posttraumatic spinal cod ischemia. J. Neurosurg. 61, 124-130.
39. Hamada Y., lkata T., Katoh S., Tsuchiya K., Niwa M., Tsutsumishita Y. and Fukuzawa K. (1996). Roles of nitric oxide in compression injury of rat spinal cord. Free Radical. Biol. Med. 20, 1-9.
40. Hara H. (1999). Involvement of caspase on apoptosis in ischemia-induced neuronal cell death: usefulness of caspase inhibitors for strokes therapy. Nippon Yakurigaku Zasshi 113, 97-111.
41. Hashimoto S., Koji T., Niu J., Kanematsu T. and Nakane P.K. (1995). Differential staining of ADN strand breaks in dying cells by non-radioactive in situ nick translation. Arch. Histol. Cytol. 58, 161-170.
42. Hoerlin B.F., Redding R.W., Hoff E.J. and McGuire J.A. (1983). Evaluation of dexamethasone, DMSO, mannitol and solcoseryl in acute spinal cord trauma. J. Am. Animal Hosp. Assoc. 19, 216-226.
43. Hoerlin B.F., Redding R.W., Hoff E.J. and McGuire J.A. (1985). Evaluation of naloxone, crocetin, TRH, methylprednisolone, partial myelotomy and hemilaminectomy in the treatment of acute spinal cord trauma. J. Am. Animal Hosp. Assoc. 21, 67-77.
44. Hurlbert R.J. (2000). Methylprednisolone for acute spinal cord injury: an inappropriate standard of care. J Neurosurg (Spine 1) 93, 1-7.
45. Isaac L. and Pejic L. (1995). Secondary mechanisms of spinal cord injury. Surg. Neurol. 43, 484-485.
46. Kanellopoulos; G.K., Kato H., Wu Y., Dougenis D., Mackey M., Hsu C.Y. and Kouchoukos N.T. (1997). Neuronal cell death in the ischemic spinal cord: the effect of methylprednisolone. Ann. Thorac. Surg. 64, 1279-1286.
47. Kaptanoglu E., Caner H.H., Surucu H.S. and Akbiyik F. (1999). Effect of mexiletine on lipid peroxidation and early ultrastructural findings in experimental spinal cord injury. J. Neurosurg. (Spine 2) 91, 200-204.
48. Kaptanoglu E., Tuncel M., Palaoglu S., Konan A., Demirpence E. and Kiling K. (2000). Comparision of the effects of melatonin and methylprednisolone in experimental spinal cord injury. J. Neurosurg.. (Spine 1) 93, 77-84.
49. Katoh K., lkata T., Katoh S., Hamada Y., Nakauchi K., Sano T. and Niwa M. (1996). Induction and its spread of apoptosis in rat spinal cord after mechanical trauma. Neurosci. Lett. 216, 9-12.
50. Kerr J.F.R., Wyllie A.H. and Currie A. (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257.
51. Kobrine A.I., Doyle T.F. and Martins A.N. (1975). Local spinal cord blood flow in experimental traumatic myelopathy. J. Neurosurg. 42, 144-149.
52. Koc P.K., Akdemir H., Karakücük E.I., Öktem I.S. and Menkü A. (1999). Effect of methylprednisolone, tirilazad mesylate and vitamin E on lipid peroxidation after experimental spinal cord injury. Spinal Cord 37, 29-32.
53. Lang B., Liu H.L., Feng G.D., Jiao X.Y. and Ju G. (2004). Astrocytes in injured adult rat spinal cord may acquire the potential of neural stem cells. Neuroscience 128, 775-783.
54. Lemke M. and Faden A.I. (11990). Edema development and ion changes in rat spinal cord after impact trauma: injury dose-response studies. J. Neurotrauma 7, 41-54.
55. Levy M.L., Gans W., Wijessinghe H.S., Soohoo W.E., Adkins R.H. and Stillerman C.B. (1996). Use of methylprednisolone as an adjunct in the management of patients with penetrating spinal cord injury: outcome analysis. Neurosurgery 39, 1141-1149.
56. Li G.L., Brodin G., Farroque M., Funa K., Holtz A., Wang W.L. and Olsson Y. (1996). Apoptosis and expression of BcI-2 after compression trauma to rat spinal cord. J. Neuropathol. Exp. Neurol. 55, 280-289.
57. Li M., Ona V.O., Chen M., Kaul M., Tennti L., Zhang X., Stieg P.E., Lipton S.A. and Friedlander R.M. (2000). Functional role and therapeutic implications of neuronal caspase-1 and -3 in a mouse model of traumatic spinal cord injury. Neuroscience 99, 333-342.
58. Li Y., Sharov V.G., Jiang N., Zaloga C., Hani N.S. and Chopp M. (11995). Untrastructural and light microscopic evidence of apoptosis after middle cerebral artery oclusion in the rat. Am. J. Pathol. 146, 1045-1050.
59. Linnik M.D., Zobrist R.H. and Hatfield, M.D. (1993). Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 24, 2002-2009.
60. Liu X.Z., Xu X.M., Hu R., Du C., Zhang J., McDonnald J.W., Dang HX, Wu Y.J., Fan J.S., Jacquin M.F., Hsu C.Y. and Choi D.W. (1997). Neuronal and glial apoptosis after traumatic spinal cord injury. J. Neurosci. 17, 5395-5406.
61. Lou J., Lenke L.G., Ludwing F.J. and O'brien M.F. (1998). Apoptosis as a mechanism of neuronal cell death following acute experimental spinal cord injury. Spinal Cord 36, 683-690.
62. Lu J., Ashwell K.W. and Waite P. (2000). Advances in secondary spinal cord injury: role of apoptosis. Spine 25, 1859-1866.
63. Nesathurai S. (1998). Steroids and spinal cord injury: revisiting the NASCIS 2 and NASCIS 3 trials. J. Trauma 45, 1088-1093.
64. Ng I., Yeo T., Tang W.Y., Soong R., Ng P.Y. and Smith D.R. (2000). Apoptosis occurs after cerebral contusion in humans. Neurosurgery 46, 949-956.
65. Ogata T., Nakamura Y., Tsuji K., Shibata T. and Kataoka K. (1993). Steroid hormones protect spinal cord neurons from glutamate toxicity. Neuroscience 55, 445-449.
66. Osterholm J.L. and Mathews G.J. (1972a). Altered metabolism following experimental spinal cord injury. Part 1: Protection againts traumatic spinal cord hemorragic necrosis by norepinephrine synthesis blockade with alpha-methyltyrosine. J. Neurosurg. 36, 386-394.
67. Osterholm J.L. and Mathews G.J. (1972b). Altered metabolism following experimental spinal cord injury. Part 11: Protection againts traumatic spinal cord hemorragic necrosis by norepinephrine synthesis blockade with alpha-methyltyrosine. J. Neurosurg. 36, 395-401.
68. Oudega M., Vargas C.G., Weber A.B., Kleitman N. and Bunge M.B. (1999). Long-term effects of methylprednisolone following transection of adult rat spinal cord. Eur. J. Neurosci. 11, 2453-2464.
69. Panter S.S., Yum S.W. and Faden A.I. (1990). Alteration in extracellular amino acids after traumatic spinal cord injury. Ann. Neurol. 27, 96-99.
70. Pointillart V., Petitjean M.E., Wiart L... Vital J.M., Lassie P., Thicoipe M. and Dabadie P. (2000). Pharmacological therapy of spinal cord injury during the acute phase. Spinal Cord 38, 71-76.
71. Saito N., Yamamoto T., Watanabe T., Abe Y. and Kumagai T. (2000). Implications of p53 protein expression in experimental spinal cord injury. J. Neurotrauma 17, 173-182.
72. Schwarch L.M. and Osborne B.A. (1993). Programmed cell death, apoptosis and killer genes. Immunol. Today 14, 582-590.
73. Short D.J., Masry W.S. and Jones P.W. (2000). High dose methylprednisolone in the management of acute spinal cord injury. A systematic review from a clinical prespective. Spinal Cord 38, 273-286.
74. Simpson R.K., Venger B.H. and Narayan R.K. (1989). Treatment of acute penetrating injuries of the spine: A retrospective analysis. J. Trauma 29, 42-46.
75. Slater A.F., Nobel S.I. and Orrenius S. (1995). The role of intracellular oxidants in apoptosis. Biochem. Biophys. Acta 1271, 59-62.
76. Song H., Stevens C.F., and Gage F. (2002). Astroglia induce neurogenesis from adult neural stem cells. Nature 417, 39-44.
77. Springer J.E., Azbill R.D. and Knapp P.E. (1999). Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury. Nat. Med. 5, 943-946.
78. Tator C.H. and Fehlings M.G. (1991). Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J. Neurosurg. 75, 15-26.
79. Tsai Y.M., Ansevin A.T. and Hnilica L.S. (1989). Association of tissue-specific histones with deoxyribinucleic acid. Thermal denaturation of native, partially dehistonized and reconstituted chromatins. Biochemistry 14, 1257-1265.
80. Vaquero J., Oya S. and Ramiro M.J. (1976). Experimental traumatic effects about myelinated fibers in the spinal cord. Invest. Clin. (Maracaibo) 17, 115-121.
81. Wyllie A.H. (1980). Glucocorticoid induced thymocyte apoptosis is associated with endogenous endonuclease activacion. Nature 284, 555-556.
82. Xu J., Fan G., Chen S., Wu S., Xu X.M. and Hsu CY. (1998). Methylprednisolone inhibition of TFN-alpha expression and NF-kB activation after spinal cord injury in rats. Brain Res. Mol. Brain Res. 59, 135-142.
83. Xu J., Kim G.M., Ahmed S.H., Xu J., Yan P., Xu X.M. and Hsu C.Y. (2001). Glucocorticoid receptor mediated suppression of activator protein-1 activation and matrix metalloproteinase expression after spinal cord injury. J. Neurosci. 21, 92-97.
84. Xu RX, Nakamura T., Nagao S., Miyamoto 0., Jin L., Toyoshima T. and Itano T. (1998). Specific inhibition of apoptosis after cold-induced brain injury by moderate postinjury hypotermia. Neurosurgery 43, 107-113.
85. Yan P., Xu J., Li Q., Chen S., Kim G.M., Hsu C.Y. and Xu X.M. (1999). Glucocorticoid receptor expression in the spinal cord after traumatic injury in adult rats. J. Neurosci. 19, 9355-9363.
86. Yong C., Arnold P.M., Zoubine M.N., Citron B.A., Watanabe I., Berman N. E. and Festoff B.W. (1998). Apoptosis in cellular compartments of rat spinal cord after severe contusion injury. J. Neurotrauma 15, 459-472.
87. Yoon D.H., Kim Y.S. and Young W. (1999). Therapeutic time window for methylprednisolone in spinal cord injured rat. Yonsei Med. J. 40, 313-320.
88. Young W. (1985). The role of calcium in spinal cord injury. CNS Trauma 2, 109-114.
89. Zhang Z., Krebs C.J. and Guth L. (1997). Experimental analysis of progressive necrosis after spinal cord trauma in the rat: etiological role of the inflammatory response. Exp. Neurol. 143, 141-152.
90. Zunino S.J., Singh M.K., Bass J. and Picker L.J. (1996). Immunodetection of histone epitopes correlates with early stages of apoptosis in activated human peripheral T-Lymphocytes. Am. J. Pathol. 149, 653-663.
91. Zurita M., Vaquero J., Oya S. and Morales C. (2002). Dexamethasone decreases apoptosis-related cell death after spinal cord injury. J. Neurosurg. (Spine) 96, 83-89.
92. Zurita M., Oya S., Morales C., López J.G., Cevallos C. and Vaquero J. (1994). Effects of dexamethasone administration on the posttraumatic demyelination in an experimental model of spinal cord contusion., In: Polytraumatized. Madrid: Mapfre Medicine, pp 343-349 [In Spanish]
93. Zurita M., Vaquero J. and Zurita I. (2001). Presence and significance of CD-95 (Fas/Apol) expression after spinal cord injury. J. Neurosurg. (Spine 2) 94, 257-264.