Neuroprotective effects of thymoquinone against spinal cord ischemia-reperfusion injury by attenuation of inflammation, oxidative stress, and apoptosis

Journal of Neurosurgery: Spine

Volumn 24, Issue 6, 2016, Pages 949-959

  Gökce, Emre Cemal ^a   Kahveci, Ramazan ^b   Gökce, Aysun ^c   Cemil, Berker ^a   Aksoy, Nurkan ^d   Sargon, Mustafa Fevzi ^e   Kisa, Üçler ^d   Erdoǧan, Bülent ^a   Güvenç, Yahya ^b   Alagöz, Fatih ^f   Kahveci, Ozan ^g  

^a TURGUT OZAL UNIVERSITY   (Turkey)

^b MINISTRY OF HEALTH   (Turkey)

^c DISKAPI YILDIRIM BEYAZIT TRAINING AND RESEARCH HOSPITAL   (Turkey)

^d KIRIKKALE UNIVERSITY   (Turkey)

^e HACETTEPE UNIVERSITY   (Turkey)

^f ANKARA TRAINING AND RESEARCH HOSPITAL   (Turkey)

^g ZONGULDAK KARAELMAS UNIVERSITY   (Turkey)

Author keywords

Apoptosis; Inflammation; Methylprednisolone; Neuroprotection; Oxidative stress; Rat; Spinal cord injury; Spinal cord ischemia reperfusion injury; Thymoquinone

Indexed keywords

CASPASE 3; CATALASE; GLUTATHIONE PEROXIDASE; INTERLEUKIN 1; MALONALDEHYDE; METHYLPREDNISOLONE; NITRIC OXIDE; SUPEROXIDE DISMUTASE; THYMOQUINONE; TUMOR NECROSIS FACTOR; ANTIOXIDANT; BENZOQUINONE DERIVATIVE; CASP3 PROTEIN, RAT; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; AORTIC OCCLUSION; APOPTOSIS; ARTICLE; BASSO BEATTIE BRESNAHAN SCALE; BLACK CUMIN; CONTROLLED STUDY; DRUG EFFICACY; HISTOPATHOLOGY; INFLAMMATION; LAPAROTOMY; LOCOMOTION; MALE; MOTONEURON; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PLANT SEED; PROTEIN EXPRESSION; RAT; RATING SCALE; REPERFUSION INJURY; SPINAL CORD INJURY; TISSUE STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; ANIMAL; DISEASE MODEL; DRUG EFFECTS; IMMUNOMODULATION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION; SPINAL CORD; SPINAL CORD ISCHEMIA; WISTAR RAT;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; BENZOQUINONES; CASPASE 3; DISEASE MODELS, ANIMAL; INTERLEUKIN-1; MALE; MALONDIALDEHYDE; MOTOR NEURONS; NEUROIMMUNOMODULATION; NEUROPROTECTIVE AGENTS; NITRIC OXIDE; OXIDATIVE STRESS; RANDOM ALLOCATION; RATS, WISTAR; REPERFUSION INJURY; SPINAL CORD; SPINAL CORD ISCHEMIA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85020261227     PISSN: 15475654     EISSN: 15475646     Source Type: Journal    
DOI: 10.3171/2015.10.SPINE15612     Document Type: Article

References (53)

1. Abdel-Zaher AO, Mostafa MG, Farghly HM, Hamdy MM, Omran GA, Al-Shaibani NK: Inhibition of brain oxidative stress and inducible nitric oxide synthase expression by thymoquinone attenuates the development of morphine tolerance and dependence in mice. Eur J Pharmacol 702:62-70, 2013
2. Al-Ali A, Alkhawajah AA, Randhawa MA, Shaikh NA: Oral and intraperitoneal LD50 of thymoquinone, an active principle of Nigella sativa, in mice and rats. J Ayub Med Coll Abbottabad 20:25-27, 2008
3. Al-Ghamdi MS: The anti-inflammatory, analgesic and antipyretic activity of Nigella sativa. J Ethnopharmacol 76:45-48, 2001
4. Ali BH, Blunden G: Pharmacological and toxicological properties of Nigella sativa. Phytother Res 17:299-305, 2003
5. Al-Majed AA, Al-Omar FA, Nagi MN: Neuroprotective effects of thymoquinone against transient forebrain ischemia in the rat hippocampus. Eur J Pharmacol 543:40-47, 2006
6. Badary OA, Taha RA, Gamal el-Din AM, Abdel-Wahab MH: Thymoquinone is a potent superoxide anion scavenger. Drug Chem Toxicol 26:87-98, 2003
7. Badr G, Mahmoud MH, Farhat K, Waly H, Al-Abdin OZ, Rabah DM: Maternal supplementation of diabetic mice with thymoquinone protects their offspring from abnormal obesity and diabetes by modulating their lipid profile and free radical production and restoring lymphocyte proliferation via PI3K/AKT signaling. Lipids Health Dis 12:37, 2013
8. Bai T, Yang Y, Wu YL, Jiang S, Lee JJ, Lian LH, et al: Thymoquinone alleviates thioacetamide-induced hepatic fibrosis and inflammation by activating LKB1-AMPK signaling pathway in mice. Int Immunopharmacol 19:351-357, 2014
9. Basso DM, Beattie MS, Bresnahan JC, Anderson DK, Faden AI, Gruner JA, et al: MASCIS evaluation of open field locomotor scores: effects of experience and teamwork on reliability. Multicenter Animal Spinal Cord Injury Study. J Neurotrauma 13:343-359, 1996
10. Bethea JR: Spinal cord injury-induced inflammation: a dualedged sword. Prog Brain Res 128:33-42, 2000
11. Bracken MB: Steroids for acute spinal cord injury. Cochrane Database Syst Rev 1:CD001046, 2012
12. Bracken MB, Collins WF, Freeman DF, Shepard MJ, Wagner FW, Silten RM, et al: Efficacy of methylprednisolone in acute spinal cord injury. JAMA 251:45-52, 1984
13. Bracken MB, Shepard MJ, Collins WF, Holford TR, Young W, Baskin DS, et al: A randomized, controlled trial of methylprednisolone or naloxone in the treatment of acute spinalcord injury. Results of the Second National Acute Spinal Cord Injury Study. N Engl J Med 322:1405-1411, 1990
14. Bracken MB, Shepard MJ, Holford TR, Leo-Summers L, Aldrich EF, Fazl M, et al: Administration of methylprednisolone for 24 or 48 hours or tirilazad mesylate for 48 hours in the treatment of acute spinal cord injury. Results of the Third National Acute Spinal Cord Injury Randomized Controlled Trial. National Acute Spinal Cord Injury Study. JAMA 277:1597-1604, 1997
15. Conrad MF, Ye JY, Chung TK, Davison JK, Cambria RP: Spinal cord complications after thoracic aortic surgery: longterm survival and functional status varies with deficit severity. J Vasc Surg 48:47-53, 2008
16. El Mezayen R, El Gazzar M, Nicolls MR, Marecki JC, Dreskin SC, Nomiyama H: Effect of thymoquinone on cyclooxygenase expression and prostaglandin production in a mouse model of allergic airway inflammation. Immunol Lett 106:72-81, 2006
17. Galaly SR, Ahmed OM, Mahmoud AM: Thymoquinone and curcumin prevent gentamicin-induced liver injury by attenuating oxidative stress, inflammation and apoptosis. J Physiol Pharmacol 65:823-832, 2014
18. Ghosheh OA, Houdi AA, Crooks PA: High performance liquid chromatographic analysis of the pharmacologically active quinones and related compounds in the oil of the black seed (Nigella sativa L.). J Pharm Biomed Anal 19:757-762, 1999
19. Hassan SA, Ahmed WA, Galeb FM, El-Taweel MA, Abu-Bedair FA: In vitro challenge using thymoquinone on hepatocellular carcinoma (HepG2) cell line. Iran J Pharm Res 7:283-290, 2008
20. Hayashi T, Sakurai M, Abe K, Sadahiro M, Tabayashi K, Itoyama Y: Apoptosis of motor neurons with induction of caspases in the spinal cord after ischemia. Stroke 29:1007-1013, 1998
21. Hosseinzadeh H, Parvardeh S, Asl MN, Sadeghnia HR, Ziaee T: Effect of thymoquinone and Nigella sativa seeds oil on lipid peroxidation level during global cerebral ischemiareperfusion injury in rat hippocampus. Phytomedicine 14:621-627, 2007
22. Houghton PJ, Zarka R, de las Heras B, Hoult JR: Fixed oil of Nigella sativa and derived thymoquinone inhibit eicosanoid generation in leukocytes and membrane lipid peroxidation. Planta Med 61:33-36, 1995
23. Huang Y, Xie K, Li J, Xu N, Gong G, Wang G, et al: Beneficial effects of hydrogen gas against spinal cord ischemiareperfusion injury in rabbits. Brain Res 1378:125-136, 2011
24. Isaksson J, Farooque M, Holtz A, Hillered L, Olsson Y: Expression of ICAM-1 and CD11b after experimental spinal cord injury in rats. J Neurotrauma 16:165-173, 1999
25. Johansson LH, Borg LA: A spectrophotometric method for determination of catalase activity in small tissue samples. Anal Biochem 174:331-336, 1988
26. Kaptanoglu E, Palaoglu S, Surucu HS, Hayran M, Beskonakli E: Ultrastructural scoring of graded acute spinal cord injury in the rat. J Neurosurg 97 (1 Suppl):49-56, 2002
27. Khan A, Vaibhav K, Javed H, Khan MM, Tabassum R, Ahmed ME, et al: Attenuation of A-induced neurotoxicity by thymoquinone via inhibition of mitochondrial dysfunction and oxidative stress. Mol Cell Biochem 369:55-65, 2012
28. Erratum in Mol Cell Biochem 376:197, 2013
29. Kruk I, Michalska T, Lichszteld K, Kładna A, Aboul-Enein HY: The effect of thymol and its derivatives on reactions generating reactive oxygen species. Chemosphere 41:1059-1064, 2000
30. Lu K, Cho CL, Liang CL, Chen SD, Liliang PC, Wang SY, et al: Inhibition of the MEK/ERK pathway reduces microglial activation and interleukin-1-beta expression in spinal cord ischemia/reperfusion injury in rats. J Thorac Cardiovasc Surg 133:934-941, 2007
31. Lutterodt H, Luther M, Salvin M, Yin JJ, Perry J, Gao JM, et al: Fatty acid profile, thymoquinone content, oxidative stability, and antioxidative properties of cold-pressed black cumin seed oils. LWT Food Sci Technol 43:1409-1413, 2011
32. Mansour MA, Nagi MN, El-Khatib AS, Al-Bekairi AM: Effects of thymoquinone on antioxidant enzyme activities, lipid peroxidation and DT-diaphorase in different tissues of mice: a possible mechanism of action. Cell Biochem Funct 20:143-151, 2002
33. Marsala M, Yaksh TL: Transient spinal ischemia in the rat: characterization of behavioral and histopathological consequences as a function of the duration of aortic occlusion. J Cereb Blood Flow Metab 14:526-535, 1994
34. Mehri S, Shahi M, Razavi BM, Hassani FV, Hosseinzadeh H: Neuroprotective effect of thymoquinone in acrylamideinduced neurotoxicity in Wistar rats. Iran J Basic Med Sci 17:1007-1011, 2014
35. Miranda KM, Espey MG, Wink DA: A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5:62-71, 2001
36. Mousavi SH, Tayarani-Najaran Z, Asghari M, Sadeghnia HR: Protective effect of Nigella sativa extract and thymoquinone on serum/glucose deprivation-induced PC12 cells death. Cell Mol Neurobiol 30:591-598, 2010
37. Nader MA, el-Agamy DS, Suddek GM: Protective effects of propolis and thymoquinone on development of atherosclerosis in cholesterol-fed rabbits. Arch Pharm Res 33:637-643, 2010
38. Nagi MN, Mansour MA: Protective effect of thymoquinone against doxorubicin-induced cardiotoxicity in rats: a possible mechanism of protection. Pharmacol Res 41:283-289, 2000
39. Nakamura M, Houghtling RA, MacArthur L, Bayer BM, Bregman BS: Differences in cytokine gene expression profile between acute and secondary injury in adult rat spinal cord. Exp Neurol 184:313-325, 2003
40. Ohkawa H, Ohishi N, Yagi K: Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351-358, 1979
41. Paglia DE, Valentine WN: Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158-169, 1967
42. Ragheb A, Elbarbry F, Prasad K, Mohamed A, Ahmed MS, Shoker A: Attenuation of the development of hypercholesterolemic atherosclerosis by thymoquinone. Int J Angiol 17:186-192, 2008
43. Reece TB, Okonkwo DO, Ellman PI, Maxey TS, Tache-Leon C, Warren PS, et al: Comparison of systemic and retrograde delivery of adenosine A2A agonist for attenuation of spinal cord injury after thoracic aortic cross-clamping. Ann Thorac Surg 81:902-909, 2006
44. Sedaghat R, Roghani M, Khalili M: Neuroprotective effect of thymoquinone, the nigella sativa bioactive compound, in 6-hydroxydopamine-induced hemi-parkinsonian rat model. Iran J Pharm Res 13:227-234, 2014
45. Sun Y, Oberley LW, Li Y: A simple method for clinical assay of superoxide dismutase. Clin Chem 34:497-500, 1988
46. Tekeoglu I, Dogan A, Ediz L, Budancamanak M, Demirel A: Effects of thymoquinone (volatile oil of black cumin) on rheumatoid arthritis in rat models. Phytother Res 21:895-897, 2007
47. Tiruppur Venkatachallam SK, Pattekhan H, Divakar S, Kadimi US: Chemical composition of Nigella sativa L. seed extracts obtained by supercritical carbon dioxide. J Food Sci Technol 47:598-605, 2010
48. Torres S, Salgado-Ceballos H, Torres JL, Orozco-Suarez S, Díaz-Ruíz A, Martínez A, et al: Early metabolic reactivation versus antioxidant therapy after a traumatic spinal cord injury in adult rats. Neuropathology 30:36-43, 2010
49. Ullah I, Ullah N, Naseer MI, Lee HY, Kim MO: Neuroprotection with metformin and thymoquinone against ethanolinduced apoptotic neurodegeneration in prenatal rat cortical neurons. BMC Neurosci 13:11, 2012
50. Umar S, Zargan J, Umar K, Ahmad S, Katiyar CK, Khan HA: Modulation of the oxidative stress and inflammatory cytokine response by thymoquinone in the collagen induced arthritis in Wistar rats. Chem Biol Interact 197:40-46, 2012
51. Vaillancourt F, Silva P, Shi Q, Fahmi H, Fernandes JC, Benderdour M: Elucidation of molecular mechanisms underlying the protective effects of thymoquinone against rheumatoid arthritis. J Cell Biochem 112:107-117, 2011
52. Woo CC, Kumar AP, Sethi G, Tan KH: Thymoquinone: potential cure for inflammatory disorders and cancer. Biochem Pharmacol 83:443-451, 2012
53. Yin F, Guo L, Meng CY, Liu YJ, Lu RF, Li P, et al: Transplantation of mesenchymal stem cells exerts anti-apoptotic effects in adult rats after spinal cord ischemia-reperfusion injury. Brain Res 1561:1-10, 2014