Anti-apoptotic and neuroprotective effects of alpha-lipoic acid on spinal cord ischemia-reperfusion injury in rabbits

Acta Neurochirurgica

Volumn 152, Issue 9, 2010, Pages 1591-1600

  Emmez, Hakan ^a   Yildirim, Zuhal ^a   Kale, Aydemir ^a   Tönge, Mehmet ^a   Durdaǧ, Emre ^a   Börcek, Alp Özgün ^a   Uçankuş, Lortlar Neşe ^a   Doǧulu, Fikret ^a   Kiliç, Nedret ^a   Baykaner, M Kemali ^a  

^a GAZI UNIVERSITY   (Turkey)

Author keywords

Ischemia reperfusion injury; Lipid peroxidation; Lipoic acid; Spinal cord injury

Indexed keywords

ADVANCED OXIDATION PROTEIN PRODUCT; CASPASE 3; GLUTATHIONE; MALONALDEHYDE; NITRIC OXIDE; SODIUM CHLORIDE; SUPEROXIDE DISMUTASE; THIOCTIC ACID;

ABDOMINAL AORTA; ANEURYSM CLIP; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTERY CLAMP; ARTICLE; CELL DEGENERATION; CELL INFILTRATION; CONTROLLED STUDY; ENZYME ACTIVITY; HISTOPATHOLOGY; INFLAMMATION; INHIBITION KINETICS; LAPAROTOMY; LUMBOSACRAL SPINE; MALE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RABBIT; RENAL ARTERY; REPERFUSION INJURY; SPINAL CORD ISCHEMIA; TREATMENT OUTCOME;

ANIMALS; APOPTOSIS; DISEASE MODELS, ANIMAL; MALE; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; RABBITS; RATS; REPERFUSION INJURY; SPINAL CORD; SPINAL CORD ISCHEMIA; THIOCTIC ACID;

EID: 77956188532     PISSN: 00016268     EISSN: 09420940     Source Type: Journal    
DOI: 10.1007/s00701-010-0703-9     Document Type: Article

References (71)

1. AP Amar ML Levy 1999 Pathogenesis and pharmacological strategies for mitigating secondary damage in acute spinal cord injury Neurosurgery 44 1027 1039 10.1097/00006123-199905000-00052 1:STN:280:DyaK1M3kslCqtA%3D%3D 10232536 discussion 1039-1040
2. G Aykac M Uysal AS Yalcin N Kocak-Toker A Sivas H Oz 1985 The effect of chronic ethanol ingestion on hepatic lipid peroxide, glutathione, glutathione peroxidase and glutathione transferase in rats Toxicology 36 71 76 10.1016/0300-483X(85)90008-3 1:CAS:528:DyaL2MXltlKqsLc%3D 4040665
3. RD Azbill X Mu AJ Bruce-Keller MP Mattson JE Springer 1997 Impaired mitochondrial function, oxidative stress and altered antioxidant enzyme activities following traumatic spinal cord injury Brain Res 765 283 290 10.1016/S0006-8993(97)00573-8 1:CAS:528:DyaK2sXks12nsLw%3D 9313901
4. DC Baptiste MG Fehlings 2006 Pharmacological approaches to repair the injured spinal cord J Neurotrauma 23 318 334 10.1089/neu.2006.23.318 16629619
5. A Bilska L Wlodek 2005 Lipoic acid-the drug of the future? Pharmacol Rep 57 570 577 1:CAS:528:DC%2BD28XktVCnuw%3D%3D 16227639
6. MP Bowes S Swanson JA Zivin 1996 The AMPA antagonist LY293558 improves functional neurological outcome following reversible spinal cord ischemia in rabbits J Cereb Blood Flow Metab 16 967 972 10.1097/00004647-199609000-00021 1:CAS:528:DyaK28XlvVKlt7k%3D 8784241
7. MB Bracken MJ Shepard TR Holford L Leo-Summers EF Aldrich M Fazl MG Fehlings DL Herr PW Hitchon LF Marshall RP Nockels V Pascale PL Perot Jr J Piepmeier VK Sonntag F Wagner JE Wilberger HR Winn W Young 1998 Methylprednisolone or tirilazad mesylate administration after acute spinal cord injury: 1-year follow up. Results of the third National Acute Spinal Cord Injury randomized controlled trial J Neurosurg 89 699 706 10.3171/jns.1998.89.5.0699 1:CAS:528:DyaK1cXnsVWqsLw%3D 9817404
8. DA Budwit-Novotny KS McCarty EB Cox JT Soper DG Mutch WT Creasman JL Flowers KS McCarty Jr 1986 Immunohistochemical analyses of estrogen receptor in endometrial adenocarcinoma using a monoclonal antibody Cancer Res 46 5419 5425 1:STN:280:DyaL2s%2Fgt1WgtQ%3D%3D 3756890
9. NE Cameron MA Cotter DH Horrobin HJ Tritschler 1998 Effects of alpha-lipoic acid on neurovascular function in diabetic rats: interaction with essential fatty acids Diabetologia 41 390 399 10.1007/s001250050921 1:CAS:528:DyaK1cXitVaqt7k%3D 9562342
10. X Cao JW Phillis 1995 The free radical scavenger, alpha-lipoic acid, protects against cerebral ischemia-reperfusion injury in gerbils Free Radic Res 23 365 370 10.3109/10715769509065257 1:CAS:528:DyaK28Xis1Ontw%3D%3D 7493042
11. AF Casini M Ferrali A Pompella E Maellaro M Comporti 1986 Lipid peroxidation and cellular damage in extrahepatic tissues of bromobenzene- intoxicated mice Am J Pathol 123 520 531 1:CAS:528:DyaL28XksFGqs7o%3D 3717304
12. P Chaudhary GH Marracci DN Bourdette 2006 Lipoic acid inhibits expression of ICAM-1 and VCAM-1 by CNS endothelial cells and T cell migration into the spinal cord in experimental autoimmune encephalomyelitis J Neuroimmunol 175 87 96 10.1016/j.jneuroim.2006.03.007 1:CAS:528:DC%2BD28XkvVOlsrk%3D 16644024
13. SD Christie B Comeau T Myers D Sadi M Purdy I Mendez 2008 Duration of lipid peroxidation after acute spinal cord injury in rats and the effect of methylprednisolone Neurosurg Focus 25 E5 10.3171/FOC.2008.25.11.E5 18980479
14. F Chronidou E Apostolakis I Papapostolou K Grintzalis CD Georgiou EN Koletsis M Karanikolas P Papathanasopoulos D Dougenis 2009 Beneficial effect of the oxygen free radical scavenger amifostine (WR-2721) on spinal cord ischemia/reperfusion injury in rabbits J Cardiothorac Surg 4 50 10.1186/1749-8090-4-50 19758462
15. A Conti M Miscusi S Cardali A Germano H Suzuki S Cuzzocrea F Tomasello 2007 Nitric oxide in the injured spinal cord: synthases cross-talk, oxidative stress and inflammation Brain Res Rev 54 205 218 10.1016/j.brainresrev.2007.01. 013 1:CAS:528:DC%2BD2sXjs1Kqtrw%3D 17500094
16. A Diaz-Ruiz C Rios I Duarte D Correa G Guizar-Sahagun I Grijalva I Madrazo A Ibarra 2000 Lipid peroxidation inhibition in spinal cord injury: cyclosporin-A vs methylprednisolone NeuroReport 11 1765 1767 10.1097/00001756-200006050-00033 1:CAS:528:DC%2BD3cXktlGitb0%3D 10852240
17. RJ Dumont DO Okonkwo S Verma RJ Hurlbert PT Boulos DB Ellegala AS Dumont 2001 Acute spinal cord injury, part I: pathophysiologic mechanisms Clin Neuropharmacol 24 254 264 10.1097/00002826-200109000-00002 1:CAS:528: DC%2BD3MXnvVGjtrs%3D 11586110
18. RJ Dumont S Verma DO Okonkwo RJ Hurlbert PT Boulos DB Ellegala AS Dumont 2001 Acute spinal cord injury, part II: contemporary pharmacotherapy Clin Neuropharmacol 24 265 279 10.1097/00002826-200109000-00003 1:CAS:528: DC%2BD3MXnvVGjtrg%3D 11586111
19. SF Erten A Kocak I Ozdemir S Aydemir A Colak BS Reeder 2003 Protective effect of melatonin on experimental spinal cord ischemia Spinal Cord 41 533 538 10.1038/sj.sc.3101508 1:STN:280:DC%2BD3svksV2htQ%3D%3D 14504608
20. T Genovese S Cuzzocrea 2008 Role of free radicals and poly(ADP-ribose)polymerase-1 in the development of spinal cord injury: new potential therapeutic targets Curr Med Chem 15 477 487 10.2174/ 092986708783503177 1:CAS:528:DC%2BD1cXnsVyisLc%3D 18289003
21. Y Gilgun-Sherki Z Rosenbaum E Melamed D Offen 2002 Antioxidant therapy in acute central nervous system injury: current state Pharmacol Rev 54 271 284 10.1124/pr.54.2.271 1:CAS:528:DC%2BD38XltVOhsr4%3D 12037143
22. PG Gunasekar AG Kanthasamy JL Borowitz GE Isom 1995 NMDA receptor activation produces concurrent generation of nitric oxide and reactive oxygen species: implication for cell death J Neurochem 65 2016 2021 10.1046/j.1471-4159.1995.65052016.x 1:CAS:528:DyaK2MXovFGmt7w%3D 7595485
23. ED Hall 1993 The role of oxygen radicals in traumatic injury: clinical implications J Emerg Med 11 Suppl 1 31 36 8445200
24. ED Hall JE Springer 2004 Neuroprotection and acute spinal cord injury: a reappraisal NeuroRx 1 80 100 10.1602/neurorx.1.1.80 15717009
25. ED Hall PA Yonkers PK Andrus JW Cox DK Anderson 1992 Biochemistry and pharmacology of lipid antioxidants in acute brain and spinal cord injury J Neurotrauma 9 Suppl 2 S425 S442 1613805
26. D Han CK Sen S Roy MS Kobayashi HJ Tritschler L Packer 1997 Protection against glutamate-induced cytotoxicity in C6 glial cells by thiol antioxidants Am J Physiol 273 R1771 R1778 1:CAS:528:DyaK2sXnsVCrtr8%3D 9374822
27. N Hosaka S Kimura A Yamazaki X Wang H Denda T Ito T Hirano N Endo 2008 Significant correlation between cerebrospinal fluid nitric oxide concentrations and neurologic prognosis in incomplete cervical cord injury Eur Spine J 17 281 286 10.1007/s00586-007-0477-9 17712576
28. CE Hulsebosch 2002 Recent advances in pathophysiology and treatment of spinal cord injury Adv Physiol Educ 26 238 255 12443996
29. F Ildan S Polat A Oner T Isbir AI Gocer O Tap M Kaya A Karadayi 1995 Effects of naloxone on sodium- and potassium-activated and magnesium-dependent adenosine-5'-triphosphatase activity and lipid peroxidation and early ultrastructural findings after experimental spinal cord injury Neurosurgery 36 797 805 10.1227/00006123-199504000-00022 1:STN:280:DyaK2MzhvFKitQ%3D%3D 7596512
30. H Kamencic RW Griebel AW Lyon PG Paterson BH Juurlink 2001 Promoting glutathione synthesis after spinal cord trauma decreases secondary damage and promotes retention of function FASEB J 15 243 250 10.1096/fj.00-0228com 1:CAS:528:DC%2BD3MXht1SnsbY%3D 11149912
31. E Kaptanoglu I Solaroglu O Okutan HS Surucu F Akbiyik E Beskonakli 2004 Erythropoietin exerts neuroprotection after acute spinal cord injury in rats: effect on lipid peroxidation and early ultrastructural findings Neurosurg Rev 27 113 120 10.1007/s10143-003-0300-y 12920606
32. M Kaymaz H Emmez N Bukan A Dursun G Kurt H Pasaoglu A Pasaoglu 2005 Effectiveness of FK506 on lipid peroxidation in the spinal cord following experimental traumatic injury Spinal Cord 43 22 26 10.1038/sj.sc.3101621 15111998
33. S Kimura N Hosaka I Yuge A Yamazaki K Suda H Taneichi H Denda N Endo 2009 Cerebrospinal fluid concentrations of nitric oxide metabolites in spinal cord injury Spine (Phila Pa 1976) 34 E645 E652
34. A Kochhar JA Zivin PD Lyden V Mazzarella 1988 Glutamate antagonist therapy reduces neurologic deficits produced by focal central nervous system ischemia Arch Neurol 45 148 153 1:STN:280:DyaL1c7jtlCgtg%3D%3D 3277597
35. RA Kowluru TS Kern RL Engerman 1997 Abnormalities of retinal metabolism in diabetes or experimental galactosemia. IV. Antioxidant defense system Free Radic Biol Med 22 587 592 10.1016/S0891-5849(96)00347-4 1:CAS:528: DyaK2sXntlyjtA%3D%3D 9013121
36. T Kristian BK Siesjo 1998 Calcium in ischemic cell death Stroke 29 705 718 1:STN:280:DyaK1c7msFClsg%3D%3D 9506616
37. H Kurtel DN Granger P Tso MB Grisham 1992 Vulnerability of intestinal interstitial fluid to oxidant stress Am J Physiol 263 G573 G578 1:CAS:528:DyaK3sXht1aitLY%3D 1415717
38. L Lang-Lazdunski C Heurteaux H Dupont C Widmann M Lazdunski 2000 Prevention of ischemic spinal cord injury: comparative effects of magnesium sulfate and riluzole J Vasc Surg 32 179 189 10.1067/mva.2000.105960 1:STN:280:DC%2BD3czjs1Ortg%3D%3D 10876221
39. OH Lowry NJ Rosebrough AL Farr RJ Randall 1951 Protein measurement with the Folin phenol reagent J Biol Chem 193 265 275 1:CAS:528:DyaG38XhsVyrsw%3D%3D 14907713
40. N Lukacova G Halat M Chavko J Marsala 1996 Ischemia-reperfusion injury in the spinal cord of rabbits strongly enhances lipid peroxidation and modifies phospholipid profiles Neurochem Res 21 869 873 10.1007/BF02532334 1:CAS:528:DyaK28XmsVejtbw%3D 8895838
41. KS McCarty Jr LS Miller EB Cox J Konrath KS McCarty Sr 1985 Estrogen receptor analyses. Correlation of biochemical and immunohistochemical methods using monoclonal antireceptor antibodies Arch Pathol Lab Med 109 716 721 3893381
42. KM Miranda MG Espey DA Wink 2001 A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite Nitric Oxide 5 62 71 10.1006/niox.2000.0319 1:CAS:528:DC%2BD3MXhtFemsrs%3D 11178938
43. Y Mitsui JD Schmelzer PJ Zollman M Mitsui HJ Tritschler PA Low 1999 Alpha-lipoic acid provides neuroprotection from ischemia-reperfusion injury of peripheral nerve J Neurol Sci 163 11 16 10.1016/S0022-510X(99)00017-9 1:CAS:528:DyaK1MXhvVGhsbg%3D 10223404
44. Y Mizuno K Ohta 1986 Regional distributions of thiobarbituric acid-reactive products, activities of enzymes regulating the metabolism of oxygen free radicals, and some of the related enzymes in adult and aged rat brains J Neurochem 46 1344 1352 10.1111/j.1471-4159.1986.tb01745.x 1:CAS:528:DyaL28Xit1ams7Y%3D 2937881
45. M Nagamatsu KK Nickander JD Schmelzer A Raya DA Wittrock H Tritschler PA Low 1995 Lipoic acid improves nerve blood flow, reduces oxidative stress, and improves distal nerve conduction in experimental diabetic neuropathy Diab Care 18 1160 1167 10.2337/diacare.18.8.1160 1:STN:280:DyaK28%2Fgt1OmtQ%3D%3D
46. HH Oruckaptan P Ozisik P Atilla M Tuncel K Kilinc PO Geyik N Basaran E Yuksel OE Ozcan 2009 Systemic administration of interleukin-10 attenuates early ischemic response following spinal cord ischemia reperfusion injury in rats J Surg Res 155 345 356 10.1016/j.jss.2008.07.013 1:CAS:528:DC%2BD1MXovF2qsrY%3D 19118842
47. L Packer HJ Tritschler K Wessel 1997 Neuroprotection by the metabolic antioxidant alpha-lipoic acid Free Radic Biol Med 22 359 378 10.1016/S0891-5849(96)00269-9 1:CAS:528:DyaK28XnsVGisr0%3D 8958163
48. M Panigrahi Y Sadguna BR Shivakumar SV Kolluri S Roy L Packer V Ravindranath 1996 alpha-Lipoic acid protects against reperfusion injury following cerebral ischemia in rats Brain Res 717 184 188 10.1016/0006-8993(96) 00009-1 1:CAS:528:DyaK28XivFKqurg%3D 8738270
49. I Pekarkova S Parara V Holecek P Stopka L Trefil J Racek R Rokyta 2001 Does exogenous melatonin influence the free radicals metabolism and pain sensation in rat? Physiol Res 50 595 602 1:CAS:528:DC%2BD38Xhslarur4%3D 11829321
50. JH Prehn C Karkoutly J Nuglisch B Peruche J Krieglstein 1992 Dihydrolipoate reduces neuronal injury after cerebral ischemia J Cereb Blood Flow Metab 12 78 87 1:CAS:528:DyaK38Xht1Sksbg%3D 1345759
51. H Qian D Liu 1997 The time course of malondialdehyde production following impact injury to rat spinal cord as measured by microdialysis and high pressure liquid chromatography Neurochem Res 22 1231 1236 10.1023/A:1021980929422 1:CAS:528:DyaK2sXmslShurc%3D 9342727
52. CK Rokkas LR Helfrich Jr DC Lobner DW Choi NT Kouchoukos 1994 Dextrorphan inhibits the release of excitatory amino acids during spinal cord ischemia Ann Thorac Surg 58 312 319 10.1016/0003-4975(94)92200-4 1:STN:280: DyaK2czks1yquw%3D%3D 7915102 discussion 319-320
53. S Roy L Packer 1998 Redox regulation of cell functions by alpha-lipoate: biochemical and molecular aspects Biofactors 8 17 21 10.1002/biof.5520080104 1:CAS:528:DyaK1cXltVGlsrc%3D 9699003
54. RD Saunders LL Dugan P Demediuk ED Means LA Horrocks DK Anderson 1987 Effects of methylprednisolone and the combination of alpha-tocopherol and selenium on arachidonic acid metabolism and lipid peroxidation in traumatized spinal cord tissue J Neurochem 49 24 31 10.1111/j.1471-4159.1987.tb03388.x 1:CAS:528:DyaL2sXktlOntrg%3D 3108455
55. RV Schillace N Pisenti N Pattamanuch S Galligan GH Marracci DN Bourdette DW Carr 2007 Lipoic acid stimulates cAMP production in T lymphocytes and NK cells Biochem Biophys Res Commun 354 259 264 10.1016/j.bbrc.2006.12.195 1:CAS:528:DC%2BD2sXhtVCltr4%3D 17210133
56. JW Schmidley 1990 Free radicals in central nervous system ischemia Stroke 21 1086 1090 1:CAS:528:DyaK3MXktVGqtrk%3D 2195717
57. K Schonheit L Gille H Nohl 1995 Effect of alpha-lipoic acid and dihydrolipoic acid on ischemia/reperfusion injury of the heart and heart mitochondria Biochim Biophys Acta 1271 335 342 1:STN:280:DyaK2MzivFCruw%3D%3D 7605800
58. E Serbinova S Khwaja AZ Reznick L Packer 1992 Thioctic acid protects against ischemia-reperfusion injury in the isolated perfused Langendorff heart Free Radic Res Commun 17 49 58 10.3109/10715769209061088 1:CAS:528: DyaK3sXpsVSjsQ%3D%3D 1446847
59. KP Shay RF Moreau EJ Smith AR Smith TM Hagen 2009 Alpha-lipoic acid as a dietary supplement: molecular mechanisms and therapeutic potential Biochim Biophys Acta 1790 1149 1160 1:CAS:528:DC%2BD1MXhtFamsr3L 19664690
60. M Skvarilova A Bulava D Stejskal S Adamovska J Bartek 2005 Increased level of advanced oxidation products (AOPP) as a marker of oxidative stress in patients with acute coronary syndrome Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 149 83 87 1:CAS:528:DC%2BD2MXhtFOjsrbM 16170393
61. AR Smith SV Shenvi M Widlansky JH Suh TM Hagen 2004 Lipoic acid as a potential therapy for chronic diseases associated with oxidative stress Curr Med Chem 11 1135 1146 1:CAS:528:DC%2BD2cXjvVehtL8%3D 15134511
62. T Sugawara A Lewen Y Gasche F Yu PH Chan 2002 Overexpression of SOD1 protects vulnerable motor neurons after spinal cord injury by attenuating mitochondrial cytochrome c release FASEB J 16 1997 1999 1:CAS:528: DC%2BD38Xps1Ojsbs%3D 12368231
63. Y Sun LW Oberley Y Li 1988 A simple method for clinical assay of superoxide dismutase Clin Chem 34 497 500 1:CAS:528:DyaL1cXhvVamt7Y%3D 3349599
64. D Taskiran FZ Kutay E Sozmen S Pogun 1997 Sex differences in nitrite/nitrate levels and antioxidant defense in rat brain NeuroReport 8 881 884 10.1097/00001756-199703030-00013 1:CAS:528:DyaK2sXivFenurs%3D 9141057
65. S-K Tsai L-M Hung Y-T Fu H Cheng M-W Nien H-Y Liu FB-Y Zhang S-S Huang 2007 Resveratrol neuroprotective effects during focal cerebral ischemia injury via nitric oxide mechanism in rats J Vasc Surg 46 346 353 10.1016/j.jvs.2007.04. 044 17600658
66. D Varija KP Kumar KP Reddy VK Reddy 2009 Prolonged constriction of sciatic nerve affecting oxidative stressors & antioxidant enzymes in rat Indian J Med Res 129 587 592 1:CAS:528:DC%2BD1MXpvV2hu7k%3D 19675389
67. V Witko-Sarsat M Friedlander C Capeillere-Blandin T Nguyen-Khoa AT Nguyen J Zingraff P Jungers B Descamps-Latscha 1996 Advanced oxidation protein products as a novel marker of oxidative stress in uremia Kidney Int 49 1304 1313 10.1038/ki.1996.186 1:CAS:528:DyaK28Xkslagsbs%3D 8731095
68. P Wolz J Krieglstein 1996 Neuroprotective effects of alpha-lipoic acid and its enantiomers demonstrated in rodent models of focal cerebral ischemia Neuropharmacology 35 369 375 10.1016/0028-3908(95)00172-7 1:CAS:528: DyaK28XjslSkur4%3D 8783212
69. M Xu GW Yip LT Gan YK Ng 2005 Distinct roles of oxidative stress and antioxidants in the nucleus dorsalis and red nucleus following spinal cord hemisection Brain Res 1055 137 142 10.1016/j.brainres.2005.07.003 1:CAS:528:DC%2BD2MXpvV2ktLc%3D 16095570
70. Yagi K (1982) Assay for serum lipid peroxide level and its clinical significance. In: Yagi K (ed) Lipid peroxides in biology and medicine. Academic, New York, pp 223-242
71. T Yoshioka K Kawada T Shimada M Mori 1979 Lipid peroxidation in maternal and cord blood and protective mechanism against activated-oxygen toxicity in the blood Am J Obstet Gynecol 135 372 376 1:CAS:528:DyaL3cXjslKl 484629