Endomorphins and morphine limit anoxia-reoxygenation-induced brain mitochondrial dysfunction in the mouse

Life Sciences

Volumn 82, Issue 13-14, 2008, Pages 752-763

  Feng, Yun ^a,b   Lu, Yingwei ^c   Lin, Xin ^a   Gao, Yanfeng ^a   Zhao, Qianyu ^a   Li, Wei ^c   Wang, Rui ^a,b  

^a North West Normal University   (China)

^b HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

^c GANSU AGRICULTURAL UNIVERSITY   (China)

Author keywords

Anoxia reoxygenation; Brain mitochondria; Endomorphins; Morphine

Indexed keywords

CARDIOLIPIN; CYTOCHROME C; ENDOMORPHIN 1; ENDOMORPHIN 2; MORPHINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN HYPOXIA; BRAIN MITOCHONDRION; CONTROLLED STUDY; DRUG INHIBITION; DRUG MECHANISM; IN VITRO STUDY; LIPID PEROXIDATION; MALE; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; REOXYGENATION; RESPIRATION CONTROL;

ANALGESICS, OPIOID; ANIMALS; BRAIN; CARDIOLIPINS; CELL HYPOXIA; CELL RESPIRATION; CYTOCHROMES C; MALE; MICE; MICE, INBRED STRAINS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; MORPHINE; OLIGOPEPTIDES; OXYGEN CONSUMPTION; RECEPTORS, OPIOID, MU; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 40649125502     PISSN: 00243205     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.lfs.2008.01.004     Document Type: Article

References (67)

1. Andreyev A., and Fiskum G. Calcium induced release of mitochondrial cytochrome c by different mechanisms selective for brain versus liver. Cell Death and Differentiation 6 9 (1999) 825-832
2. Barry U., and Zuo Z. Opioids: old drugs for potential new applications. Current Pharmaceutical Design 11 10 (2005) 1343-1350
3. Benzel E.C., Musgrove II C.C., and Kesterson L. Naloxone and mortality in the gerbil stroke model. Southern Medical Journal 82 5 (1989) 555-557
4. 5) enkephalin: linking hibernation and neuroprotection. Frontiers in Bioscience 9 (2004) 3392-3398
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 (1976) 248-254
6. Cadenas E., and Davies K.J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radical Biology and Medicine 29 3-4 (2000) 222-230
7. Chang W.L., Lee S.S., and Su M.J. Attenuation of post-ischemia reperfusion injury by thaliporphine and morphine in rat hearts. Journal of Biomedical Science 12 4 (2005) 611-619
8. + homeostasis during anoxia and oxygen-glucose deprivation. Journal of Cerebral Blood Flow and Metabolism 27 2 (2007) 356-368
9. Charron, C., Messier, C., Plamondon, H., in press. Neuroprotection and functional recovery conferred by administration of kappa- and delta1-opioid agonists in a rat model of global ischemia. Physiology and Behavior. doi:10.1016/j.physbeh.2007.10.015.
10. Coccia R., Foppoli C., Blarzino C., Marco C.D., and Rosei M.A. Interaction of enkephalin derivatives with reactive oxygen species. Biochimica et Biophysica Acta 1525 1-2 (2001) 43-49
11. Cormier A., Morin C., Zini R., Tillement J.P., and Lagrue G. Nicotine protects rat brain mitochondria against experimental injuries. Neuropharmacology 44 5 (2003) 642-652
12. Das N.P., and Ratty A.K. Studies on the effects of the narcotic alkaloids, cocaine, morphine, and codeine on nonenzymatic lipid peroxidation in rat brain mitochondria. Biochemical Medicine and Metabolic Biology 37 2 (1987) 258-264
13. Demel R.A., Jordi W., Lambrechts H., Van Damme H., Hovius R., and De Kruijff B. Differential interactions of apo- and holocytochrome c with acidic membrane lipids in model systems and the implications for their import into mitochondria. Journal of Biological Chemistry 264 7 (1989) 3988-3997
14. Du G., Mouithys-Mickalad A., and Sluse F.E. Generation of superoxide anion by mitochondria and impairment of their functions during anoxia and reoxygenation in vitro. Free Radical Biology and Medicine 25 9 (1998) 1066-1074
15. Du G., Willet K., Mouithys-Mickalad A., Sluse-Goffart M., Droy-Lefaix M.T., and Sluse F.E. EGb 761 protects liver mitochondria against injury induced by in vitro anoxia/reoxygenation. Free Radical Biology and Medicine 27 5-6 (1999) 596-604
16. Du G., Willet K., Jarmuszkiewicz W., Sluse-Goffart C.M., and Sluse F.E. Protective effect of EGb 761 against oxidative phosphorylation of brain mitochondria after anoxia/reoxygenation in vivo and in vitro. Toxicology Mechanisms and Methods 14 1-2 (2004) 97-101
17. Fiskum G., Murphy A.N., and Beal M.F. Mitochondria in neurodegeneration: acute ischemia and chronic neurodegenerative diseases. Journal of Cerebral Blood Flow and Metabolism 19 4 (1999) 351-369
18. Floyd R.A. Antioxidants, oxidative stress, and degenerative neurological disorders. Proceedings of the Society for Experimental Biology and Medicine 222 3 (1999) 236-245
19. Floyd R.A., and Hensley K. Oxidative stress in brain aging-implications for therapeutics of neurodegenerative diseases. Neurobiology of Aging 23 5 (2002) 795-807
20. Fontana M., Mosca L., and Rosei M.A. Interaction of enkephalins with oxyradicals. Biochemical Pharmacology 61 10 (2001) 1253-1257
21. Formisano L., Noh K.M., Miyawaki T., Mashiko T., Bennett M.V., and Zukin R.S. Ischemic insults promote epigenetic reprogramming of mu opioid receptor expression in hippocampal neurons. Proceedings of the National Academy of Sciences 104 10 (2007) 4170-4175
22. Frässdorf J., Weber N.C., Obal D., Toma O., Müllenheim J., Kojda G., Preckel B., and Schlack W. Morphine induces late cardioprotection in rat hearts in vivo: the involvement of opioid receptors and nuclear transcription factor kappaB. Anesthesia and Analgesia 101 4 (2005) 934-941
23. Gabbita S.P., Subramaniam R., Allouch F., Carney J.M., and Butterfield D.A. Effects of mitochondrial respiratory stimulation on membrane lipids and proteins: an electron paramagnetic resonance investigation. Biochimica et Biophysica Acta 1372 2 (1998) 163-173
24. 2+-independent mechanisms that are regulated by Bax. Journal of Biological Chemistry 276 22 (2001) 19066-19071
25. Green D.R., and Reed J.C. Mitochondria and apoptosis. Science 281 5381 (1998) 1309-1312
26. Gulcin I., Beydemir S., Alici H.A., Elmastas M., and Buyukokuroglu M.E. In vitro antioxidant properties of morphine. Pharmacological Research 49 1 (2004) 59-66
27. Hayakawa M., Ogawa T., Sugiyama S., and Ozawa T. Hydroxyl radical and leukotoxin biosynthesis in neutrophil plasma membrane. Biochemical and Biophysical Research Communications 161 3 (1989) 1077-1085
28. Iwata M., Inoue S., Kawaguchi M., Nakamura M., Konishi N., and Furuya H. Effects of delta-opioid receptor stimulation and inhibition on hippocampal survival in a rat model of forebrain ischaemia. British Journal of Anaesthesia 99 4 (2007) 538-546
29. Jacobson J., Duchen M.R., and Heales S.J. Intracellular distribution of the fluorescent dye nonyl acridine orange responds to the mitochondrial membrane potential: implications for assays of cardiolipin and mitochondrial mass. Journal of Neurochemistry 82 2 (2002) 224-233
30. Jessop D.S., Richards L.J., and Harbuz M.S. Opioid peptides endomorphin-1 and endomorphin-2 in the immune system in humans and in a rodent model of inflammation. Annals of the New York Academy of Sciences 966 (2002) 456-463
31. Kim M.S., Cheong Y.P., So H.S., Lee K.M., Kim T.Y., Oh J., Chung Y.T., Son Y., Kim B.R., and Park R. Protective effects of morphine in peroxynitrite-induced apoptosis of primary rat neonatal astrocytes: potential involvement of G protein and phosphatidylinositol 3-kinase (PI3 kinase). Biochemical Pharmacology 61 7 (2001) 779-786
32. Kirkland R.A., Adibhatla R.M., Hatcher J.F., and Franklin J.L. Loss of cardiolipin and mitochondria during programmed neuronal death: evidence of a role for lipid peroxidation and autophagy. Neuroscience 115 2 (2002) 587-602
33. Kluck R.M., Bossy-Wetzel E., Green D.R., and Newmeyer D.D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275 5303 (1997) 1132-1136
34. Kofke W.A., Garman R.H., Garman R., and Rose M.E. Opioid neurotoxicity: fentanyl-induced exacerbation of cerebral ischemia in rats. Brain Research 818 2 (1999) 326-334
35. Lee C.P. Biochemical studies of isolated mitochondria from normal and diseased tissues. Biochimica et Biophysica Acta 1271 1 (1995) 21-28
36. Lenaz G. Role of mitochondria in oxidative stress and ageing. Biochimica et Biophysica Acta 1366 1-2 (1998) 53-67
37. León J., Acuña-Castroviejo D., Sainz R.M., Mayo J.C., Tan D.X., and Reiter R.J. Melatonin and mitochondrial function. Life Sciences 75 7 (2004) 765-790
38. León J., Acuña-Castroviejo D., Escames G., Tan D.X., and Reiter R.J. Melatonin mitigates mitochondrial malfunction. Journal of Pineal Research 38 1 (2005) 1-9
39. Liao S.L., Chen W.Y., Raung S.L., and Chen C.J. Neuroprotection of naloxone against ischemic injury in rats: role of mu receptor antagonism. Neuroscience Letters 345 3 (2003) 169-172
40. Lim Y.J., Zheng S., and Zuo Z. Morphine preconditions Purkinje cells against cell death under in vitro simulated ischemia-reperfusion conditions. Anesthesiology 100 3 (2004) 562-568
41. Lin X., Yang D.J., Cai W.Q., Zhao Q.Y., Gao Y.F., Chen Q., and Wang R. Endomorphins, endogenous opioid peptides, provide antioxidant defense in the brain against free radical-induced damage. Biochimica et Biophysica Acta 1639 3 (2003) 195-202
42. Lin X., Xue L.Y., Wang R., Zhao Q.Y., and Chen Q. Protective effects of endomorphins, endogenous opioid peptides in the brain, on human low density lipoprotein oxidation. FEBS Journal 273 6 (2006) 1275-1284
43. Liu J., and Mori A. Monoamine metabolism provides an antioxidant defense in the brain against oxidant- and free radical-induced damage. Archives of Biochemistry and Biophysics 302 1 (1993) 118-127
44. Liu Y., Fiskum G., and Schubert D. Generation of reactive oxygen species by the mitochondrial electron transport chain. Journal of Neurochemistry 80 5 (2002) 780-787
45. McIntosh T.K., Fernyak S., Hayes R.L., and Faden A.I. Beneficial effect of the nonselective opiate antagonist naloxone hydrochloride and the thyrotropin-releasing hormone (TRH) analog YM-14673 on long-term neurobehavioral outcome following experimental brain injury in the rat. Journal of Neurotrauma 10 4 (1993) 373-384
46. Mecocci P., Beal M.F., Cecchetti R., Polidori M.C., Cherubini A., Chionne F., Avellini L., Romano G., and Senin U. Mitochondrial membrane fluidity and oxidative damage to mitochondrial DNA in aged and AD human brain. Molecular and Chemical Neuropathology 31 1 (1997) 53-64
47. Morin C., Zini R., Simon N., and Tillement J.P. Dehydroepiandrosterone and alpha-estradiol limit the functional alterations of rat brain mitochondria submitted to different experimental stresses. Neuroscience 115 2 (2002) 415-424
48. Morin C., Zini R., and Tillement J.P. Anoxia-reoxygenation-induced cytochrome c and cardiolipin release from rat brain mitochondria. Biochemical and Biophysical Research Communications 307 3 (2003) 477-482
49. Nomura K., Imai H., Koumura T., Kobayashi T., and Nakagawa Y. Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemiainduced apoptosis. Biochemical Journal 351 Pt 1 (2000) 183-193
50. Okubo S., Tanabe Y., Takeda K., Kitayama M., Kanemitsu S., Kukreja R.C., and Takekoshi N. Ischemic preconditioning and morphine attenuate myocardial apoptosis and infarction after ischemia-reperfusion in rabbits: role of delta-opioid receptor. American Journal of Physiology Heart and Circulatory Physiology 287 4 (2004) H1786-H1791
51. Peart J.N., and Gross G.J. Cardioprotective effects of acute and chronic opioid treatment are mediated via different signaling pathways. American Journal of Physiology Heart and Circulatory Physiology 291 4 (2006) H1746-H1753
52. Peart J.N., Gross E.R., and Gross G.J. Opioid-induced preconditioning: recent advances and future perspectives. Vascular Pharmacology 42 5-6 (2005) 211-218
53. Ricchelli F., Gobbo S., Moreno G., and Salet C. Changes of fluidity of mitochondrial membranes induced by the permeability transition. Biochemistry 38 29 (1999) 9295-9300
54. Rubaj A., Gustaw K., Zgodziński W., Kleinrok Z., and Sieklucka-Dziuba M. The role of opioid receptors in hypoxic preconditioning against seizures in brain. Pharmacology Biochemistry and Behavior 67 1 (2000) 65-70
55. Salmasi A.H., Beheshtian A., Payabvash S., Demehri S., Ebrahimkhani M.R., Karimzadegan M., Bahadori M., Pasalar P., and Dehpour A.R. Effect of morphine on ischemia-reperfusion injury: experimental study in testicular torsion rat model. Urology 66 6 (2005) 1338-1342
56. Sims N.R. Rapid isolation of metabolically active mitochondria from rat brain and subregions using Percoll density gradient centrifugation. Journal of Neurochemistry 55 2 (1990) 698-707
57. Skulachev V.P. Uncoupling: new approaches to an old problem of bioenergetics. Biochimica et Biophysica Acta 1363 2 (1998) 100-124
58. Sperka-Gottlieb C.D., Hermetter A., Paltauf F., and Daum G. Lipid topology and physical properties of the outer mitochondrial membrane of the yeast, Saccharomyces cerevisiae. Biochimica et Biophysica Acta 946 2 (1988) 227-234
59. 5]enkephalin promotes cell survival. Journal of Biomedical Science 7 3 (2000) 195-199
60. 5] enkephalin in neuronal death and retarded behavior induced by forebrain ischemia in rats. Neuroscience Letters 423 2 (2007) 113-117
61. Wu D., Soong Y., Zhao G.M., and Szeto H.H. A highly potent peptide analgesic that protects against ischemia-reperfusion-induced myocardial stunning. American Journal of Physiology Heart and Circulatory Physiology 283 2 (2002) H783-H791
62. Zabramski J.M., Spetzler R.F., Selman W.R., Roessmann U.R., Hershey L.A., Crumrine R.C., and Macko R. Naloxone therapy during focal cerebral ischemia evaluation in a primate model. Stroke 15 4 (1984) 621-627
63. Zadina J.E., Hackler L., Ge L.J., and Kastin A.J. A potent and selective endogenous agonist for the mu-opiate receptor. Nature 386 6624 (1997) 499-502
64. Zhang M., Mileykovskaya E., and Dowhan W. Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria. Journal of Biological Chemistry 280 33 (2005) 29403-29408
65. 2, display partial agonist potency but significant antinociception. Life Sciences 77 10 (2005) 1155-1165
66. Zhao P., Huang Y., and Zuo Z. Opioid preconditioning induces opioid receptor-dependent delayed neuroprotection against ischemia in rats. Journal of Neuropathology & Experimental Neurology 65 10 (2006) 945-952
67. Zini R., Morin C., Bertelli A., Bertelli A.A., and Tillement J.P. Resveratrol-induced limitation of dysfunction of mitochondria isolated from rat brain in an anoxia-reoxygenation model. Life Sciences 71 26 (2002) 3091-3108