Osthole attenuates spinal cord ischemiaereperfusion injury through mitochondrial biogenesiseindependent inhibition of mitochondrial dysfunction in rats

Journal of Surgical Research

Volumn 185, Issue 2, 2013, Pages 805-814

  Zhou, Yue Fei ^a   Li, Liang ^a   Feng, Feng ^b   Yuan, Hua ^a   Gao, Da Kuan ^a   Fu, Luo An ^a   Fei, Zhou ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Ischemiaereperfusion injury; Mitochondria; Neuroprotection; Oxidative stress

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C; MITOCHONDRIAL DNA; OSTHOLE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR; CALCIUM CHANNEL BLOCKING AGENT; COUMARIN DERIVATIVE; HERBACEOUS AGENT; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOGENESIS; BRAIN FUNCTION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOTONEURON; MOTOR PERFORMANCE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT; REPERFUSION INJURY; RESPIRATORY CHAIN; SPINAL CORD; SPINAL CORD ISCHEMIA; WATER CONTENT; ANIMAL; CHEMISTRY; CNIDIUM; DRUG EFFECTS; HEMODYNAMICS; METABOLISM; MITOCHONDRIAL DISEASES; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; SPINAL CORD INJURIES; SPRAGUE DAWLEY RAT; DRUG EFFECT; ISCHEMIA-REPERFUSION INJURY; SPINAL CORD INJURY;

ANIMALS; CALCIUM CHANNEL BLOCKERS; CNIDIUM; COUMARINS; DRUGS, CHINESE HERBAL; HEMODYNAMICS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL DISEASES; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; SPINAL CORD INJURIES;

ISCHEMIA-REPERFUSION INJURY; MITOCHONDRIA; NEUROPROTECTION; OXIDATIVE STRESS;

EID: 84891669212     PISSN: 00224804     EISSN: 10958673     Source Type: Journal    
DOI: 10.1016/j.jss.2013.06.044     Document Type: Article

References (56)

1. Pouw MH, Hosman AJ, van Kampen A, Hirschfeld S, Thietje R, van de Meent H. Is the outcome in acute spinal cord ischaemia different from that in traumatic spinal cord injury? A cross-sectional analysis of the neurological and functional outcome in a cohort of 93 paraplegics. Spinal Cord 2011;49:307-12.
2. Guerit JM, Dion RA. State-of-the-art of neuromonitoring for prevention of immediate and delayed paraplegia in thoracic and thoracoabdominal aorta surgery. Ann Thorac Surg 2002; 74:S1867-9. discussion S1892-1868.
3. Wan IY, Angelini GD, Bryan AJ, Ryder I, Underwood MJ. Prevention of spinal cord ischaemia during descending thoracic and thoracoabdominal aortic surgery. Eur J Cardiothorac Surg 2001;19:203-13.
4. Matsuda H, Fukuda T, Iritani O, et al. Spinal cord injury is not negligible after TEVAR for lower descending aorta. Eur J Vasc Endovasc Surg 2010;39:179-86.
5. Zhu JW, Chen T, Guan J, Liu WB, Liu J. Neuroprotective effects of allicin on spinal cord ischemia-reperfusion injury via improvement of mitochondrial function in rabbits. Neurochem Int 2012;61:640-8.
6. Peppelenbosch AG, Vermeulen Windsant IC, Jacobs MJ, Tordoir JH, Schurink GW. Open repair for ruptured abdominal aortic aneurysm and the risk of spinal cord ischemia: review of the literature and risk-factor analysis. Eur J Vasc Endovasc Surg 2010;40:589-95.
7. de Haan P. Pharmacologic adjuncts to protect the spinal cord during transient ischemia. Semin Vasc Surg 2000;13:264-71.
8. de Haan P, Kalkman CJ, Jacobs MJ. Pharmacologic neuroprotection in experimental spinal cord ischemia: a systematic review. J Neurosurg Anesthesiol 2001;13:3-12.
9. McBride HM, Neuspiel M, Wasiak S. Mitochondria: more than just a powerhouse. Curr Biol 2006;16:R551-60.
10. Li T, Zhang P, Liu J, et al. Protective effects of hemoglobin-based oxygen carrier given to isolated heart during ischemia via attenuation of mitochondrial oxidative damage. Free Radic Biol Med 2010;48:1079-89.
11. Aldakkak M, Camara AK, Heisner JS, Yang M, Stowe DF. Ranolazine reduces Ca2+ overload and oxidative stress and improves mitochondrial integrity to protect against ischemia reperfusion injury in isolated hearts. Pharmacol Res 2011;64: 381-92.
12. Ko FN, Wu TS, Liou MJ, Huang TF, Teng CM. Vasorelaxation of rat thoracic aorta caused by osthole isolated from Angelica pubescens. Eur J Pharmacol 1992;219:29-34.
13. Okamoto T, Kawasaki T, Hino O. Osthole prevents anti-Fas antibody-induced hepatitis in mice by affecting the caspase-3-mediated apoptotic pathway. Biochem Pharmacol 2003;65: 677-81.
14. Chou SY, Hsu CS, Wang KT, Wang MC, Wang CC. Antitumor effects of Osthol from Cnidium monnieri: an in vitro and in vivo study. Phytother Res 2007;21:226-30.
15. Nakamura T, Kodama N, Arai Y, et al. Inhibitory effect of oxycoumarins isolated from the Thai medicinal plant Clausena guillauminii on the inflammation mediators, iNOS, TNF-alpha, and COX-2 expression in mouse macrophage RAW 264.7. J Nat Med 2009;63:21-7.
16. Matsuda H, Tomohiro N, Ido Y, Kubo M. Anti-allergic effects of cnidii monnieri fructus (dried fruits of Cnidium monnieri) and its major component, osthol. Biol Pharm Bull 2002;25: 809-12.
17. Li XX, Hara I, Matsumiya T. Effects of osthole on postmenopausal osteoporosis using ovariectomized rats; comparison to the effects of estradiol. Biol Pharm Bull 2002; 25:738-42.
18. Luszczki JJ, Wojda E, Andres-Mach M, et al. Anticonvulsant and acute neurotoxic effects of imperatorin, osthole and valproate in the maximal electroshock seizure and chimney tests in mice: a comparative study. Epilepsy Res 2009;85:293-9.
19. Liang HJ, Suk FM, Wang CK, et al. Osthole, a potential antidiabetic agent, alleviates hyperglycemia in db/db mice. Chem Biol Interact 2009;181:309-15.
20. Guh JH, Yu SM, Ko FN, Wu TS, Teng CM. Antiproliferative effect in rat vascular smooth muscle cells by osthole, isolated from Angelica pubescens. Eur J Pharmacol 1996;298: 191-7.
21. Chao X, Zhou J, Chen T, et al. Neuroprotective effect of osthole against acute ischemic stroke on middle cerebral ischemia occlusion in rats. Brain Res 2010;1363:206-11.
22. Chen T, Liu W, Chao X, et al. Neuroprotective effect of osthole against oxygen and glucose deprivation in rat cortical neurons: involvement of mitogen-activated protein kinase pathway. Neuroscience 2011;183:203-11.
23. He Y, Qu S, Wang J, et al. Neuroprotective effects of osthole pretreatment against traumatic brain injury in rats. Brain Res 2012;1433:127-36.
24. Lu K, Liang CL, Liliang PC, et al. Inhibition of extracellular signal-regulated kinases 1/2 provides neuroprotection in spinal cord ischemia/reperfusion injury in rats: relationship with the nuclear factor-kappaB-regulated anti-apoptotic mechanisms. J Neurochem 2010;114:237-46.
25. Die J, Wang K, Fan L, Jiang Y, Shi Z. Rosuvastatin preconditioning provides neuroprotection against spinal cord ischemia in rats through modulating nitric oxide synthase expressions. Brain Res 2010;1346:251-61.
26. Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 1995;12:1-21.
27. Morin C, Zini R, Simon N, Tillement JP. Dehydroepiandrosterone and alpha-estradiol limit the functional alterations of rat brain mitochondria submitted to different experimental stresses. Neuroscience 2002;115: 415-24.
28. Chen H, Hu CJ, He YY, Yang DI, Xu J, Hsu CY. Effects of emodin treatment on mitochondrial ATP generation capacity and antioxidant components as well as susceptibility to ischemia-reperfusion injury in rat hearts: single versus multiple doses and gender difference. Life Sci 2005;77: 2770-82.
29. Chen H, Hu CJ, He YY, Yang DI, Xu J, Hsu CY. Reduction and restoration of mitochondrial dna content after focal cerebral ischemia/reperfusion. Stroke 2001;32:2382-7.
30. Estornell E, Fato R, Pallotti F, Lenaz G. Assay conditions for the mitochondrial NADH:coenzyme Q oxidoreductase. FEBS Lett 1993;332:127-31.
31. Dave KR, DeFazio RA, Raval AP, et al. Ischemic preconditioning targets the respiration of synaptic mitochondria via protein kinase C epsilon. J Neurosci 2008;28:4172-82.
32. Krahenbuhl S, Chang M, Brass EP, Hoppel CL. Decreased activities of ubiquinol:ferricytochrome c oxidoreductase (complex III) and ferrocytochrome c:oxygen oxidoreductase (complex IV) in liver mitochondria from rats with hydroxycobalamin[c-lactam]-induced methylmalonic aciduria. J Biol Chem 1991;266:20998-1003.
33. Liu WB, Zhou J, Qu Y, et al. Neuroprotective effect of osthole on MPP+-induced cytotoxicity in PC12 cells via inhibition of mitochondrial dysfunction and ROS production. Neurochem Int 2010;57:206-15.
34. Chen R, Xue J, Xie ML. Reduction of isoprenaline-induced myocardial TGF-beta1 expression and fibrosis in osthole-treated mice. Toxicol Appl Pharmacol 2011;256:168-73.
35. Ley JJ, Belayev L, Saul I, Becker DA, Ginsberg MD. Neuroprotective effect of STAZN, a novel azulenyl nitrone antioxidant, in focal cerebral ischemia in rats: dose-response and therapeutic window. Brain Res 2007;1180: 101-10.
36. Ye R, Kong X, Yang Q, Zhang Y, Han J, Zhao G. Ginsenoside Rd attenuates redox imbalance and improves stroke outcome after focal cerebral ischemia in aged mice. Neuropharmacology 2011;61:815-24.
37. Bjelakovic G, Nikolova D, Gluud LL, Simonetti RG, Gluud C. Mortality in randomized trials of antioxidant supplements for primary and secondary prevention: systematic review and meta-analysis. JAMA 2007;297:842-57.
38. Villmann C, Becker CM. On the hypes and falls in neuroprotection: targeting the NMDA receptor. Neuroscientist 2007;13:594-615.
39. Fisher M, Hachinski V. European Cooperative Acute Stroke Study III: support for and questions about a truly emerging therapy. Stroke 2009;40:2262-3.
40. Fisher M, Feuerstein G, Howells DW, et al. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 2009;40:2244-50.
41. Kurokawa T, Takagi H. Mechanism and prevention of ischemia-reperfusion injury. Transplant Proc 1999;31: 1775-6.
42. Vajdovich P. Free radicals and antioxidants in inflammatory processes and ischemia-reperfusion injury. Vet Clin North Am Small Anim Pract 2008;38:31-123. v.
43. Siemionow M, Arslan E. Ischemia/reperfusion injury: a review in relation to free tissue transfers. Microsurgery 2004;24:468-75.
44. Cadenas E, Davies KJ. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 2000;29: 222-30.
45. Lemasters JJ, Theruvath TP, Zhong Z, Nieminen AL. Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta 2009;1787:1395-401.
46. Leonard JV, Schapira AH. Mitochondrial respiratory chain disorders I: mitochondrial DNA defects. Lancet 2000;355: 299-304.
47. Lestienne P. Mitochondrial and nuclear DNA complementation in the respiratory chain function and defects. Biochimie 1989;71:1115-23.
48. Zhang Q, Wu Y, Zhang P, et al. Exercise induces mitochondrial biogenesis after brain ischemia in rats. Neuroscience 2012;205:10-7.
49. McLeod CJ, Pagel I, Sack MN. The mitochondrial biogenesis regulatory program in cardiac adaptation to ischemiaea putative target for therapeutic intervention. Trends Cardiovasc Med 2005;15:118-23.
50. Cheng A, Hou Y, Mattson MP. Mitochondria and neuroplasticity. ASN Neuro 2010;2:e00045.
51. Ljubicic V, Joseph AM, Saleem A, et al. Transcriptional and post-transcriptional regulation of mitochondrial biogenesis in skeletal muscle: effects of exercise and aging. Biochim Biophys Acta 2010;1800:223-34.
52. Vina J, Gomez-Cabrera MC, Borras C, et al. Mitochondrial biogenesis in exercise and in ageing. Adv Drug Deliv Rev 2009;61:1369-74.
53. Islam R, Yang L, Sah M, et al. A neuroprotective role of the human uncoupling protein 2 (hUCP2) in a Drosophila Parkinson's disease model. Neurobiol Dis 2012;46:137-46.
54. Robinson BH. Human complex I deficiency: clinical spectrum and involvement of oxygen free radicals in the pathogenicity of the defect. Biochim Biophys Acta 1998;1364:271-86.
55. Kudin AP, Kudina TA, Seyfried J, et al. Seizure-dependent modulation of mitochondrial oxidative phosphorylation in rat hippocampus. Eur J Neurosci 2002;15:1105-14.
56. Kushnareva Y, Murphy AN, Andreyev A. Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation-reduction state. Biochem J 2002;368:545-53.