Methadone induces necrotic-like cell death in SH-SY5Y cells by an impairment of mitochondrial ATP synthesis

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1802, Issue 11, 2010, Pages 1036-1047

  Perez Alvarez, Sergio ^a   Cuenca Lopez, Maria D ^a   de Mera, Raquel M Melero Fernández ^a   Puerta, Elena ^b   Karachitos, Andonis ^c   Bednarczyk, Piotr ^d   Kmita, Hanna ^c   Aguirre, Norberto ^b   Galindo, Maria F ^e   Jordán, Joaquin ^a,f  

^a UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

^c ADAM MICKIEWICZ UNIVERSITY   (Poland)

^d WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

^e HOSPITAL GENERAL UNIVERSITARIO DE ALBACETE   (Spain)

^f Neurological Disabilities Research Institute   (Spain)

Author keywords

Bax; Clark electrode; Methadone; Mitochondria; Necrosis; Neurodegeneration

Indexed keywords

ADENOSINE TRIPHOSPHATE; CASPASE; CYTOCHROME C; METHADONE; PROTEIN BAX; PROTEIN BCL XL; PROTEIN P53;

ARTICLE; BIOENERGY; CELL DEATH; CELL ENERGY; CONTROLLED STUDY; DRUG ACTIVITY; ENZYME RELEASE; HUMAN; HUMAN CELL; LIVER MITOCHONDRION; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; OXIDATIVE PHOSPHORYLATION UNCOUPLING; PRIORITY JOURNAL; PROTEIN TRANSPORT;

ANALGESICS, OPIOID; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CALCIUM; CASPASES; CELL LINE, TUMOR; CELL SURVIVAL; CELLS, CULTURED; CYTOCHROMES C; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX II; HUMANS; METHADONE; MICE; MICE, KNOCKOUT; MITOCHONDRIA, LIVER; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; NECROSIS; NEUROBLASTOMA; PROTEIN TRANSPORT; RATS; REACTIVE OXYGEN SPECIES;

RATTUS;

EID: 77956647666     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2010.07.024     Document Type: Article

References (57)

1. Krantz M.J., Mehler P.S. Treating opioid dependence. Growing implications for primary care. Arch Intern Med 2004, 164:277-288.
2. Mercadante S. Opioid titration in cancer pain: a critical review. Eur J Pain 2007, 11:823-830.
3. Mercadante S. Methadone in cancer pain. Eur J Pain 1997, 1:77-83. discussion 84-75.
4. Friesen C., Roscher M., Alt A., Miltner E. Methadone, commonly used as maintenance medication for outpatient treatment of opioid dependence, kills leukemia cells and overcomes chemoresistance. Cancer Res 2008, 68:6059-6064.
5. Papageorgiou C.C., Liappas I.A., Ventouras E.M., Nikolaou C.C., Kitsonas E.N., Uzunoglu N.K., Rabavilas A.D. Long-term abstinence syndrome in heroin addicts: indices of P300 alterations associated with a short memory task. Prog Neuropsychopharmacol Biol Psychiatry 2004, 28:1109-1115.
6. Guerra D., Sole A., Cami J., Tobena A. Neuropsychological performance in opiate addicts after rapid detoxification. Drug Alcohol Depend 1987, 20:261-270.
7. Verdejo A., Toribio I., Orozco C., Puente K.L., Perez-Garcia M. Neuropsychological functioning in methadone maintenance patients versus abstinent heroin abusers. Drug Alcohol Depend 2005, 78:283-288.
8. Gritz E.R., Shiffman S.M., Jarvik M.E., Haber J., Dymond A.M., Coger R., Charuvastra V., Schlesinger J. Physiological and psychological effects of methadone in man. Arch Gen Psychiatry 1975, 32:237-242.
9. Darke S., Sims J., McDonald S., Wickes W. Cognitive impairment among methadone maintenance patients. Addiction 2000, 95:687-695.
10. Specka M., Finkbeiner T., Lodemann E., Leifert K., Kluwig J., Gastpar M. Cognitive-motor performance of methadone-maintained patients. Eur Addict Res 2000, 6:8-19.
11. Curran H.V., Kleckham J., Bearn J., Strang J., Wanigaratne S. Effects of methadone on cognition, mood and craving in detoxifying opiate addicts: a dose-response study. Psychopharmacology (Berl) 2001, 154:153-160.
12. Kornreich C., Foisy M.L., Philippot P., Dan B., Tecco J., Noel X., Hess U., Pelc I., Verbanck P. Impaired emotional facial expression recognition in alcoholics, opiate dependence subjects, methadone maintained subjects and mixed alcohol-opiate antecedents subjects compared with normal controls. Psychiatry Res 2003, 119:251-260.
13. Mintzer M.Z., Stitzer M.L. Cognitive impairment in methadone maintenance patients. Drug Alcohol Depend 2002, 67:41-51.
14. Bruera E., Macmillan K., Hanson J., MacDonald R.N. The cognitive effects of the administration of narcotic analgesics in patients with cancer pain. Pain 1989, 39:13-16.
15. Vainio A., Ollila J., Matikainen E., Rosenberg P., Kalso E. Driving ability in cancer patients receiving long-term morphine analgesia. Lancet 1995, 346:667-670.
16. Galski T., Williams J.B., Ehle H.T. Effects of opioids on driving ability. J Pain Symptom Manage 2000, 19:200-208.
17. Haythornthwaite J.A., Menefee L.A., Quatrano-Piacentini A.L., Pappagallo M. Outcome of chronic opioid therapy for non-cancer pain. J Pain Symptom Manage 1998, 15:185-194.
18. Leist M., Jaattela M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2001, 2:589-598.
19. Tymianski M., Charlton M.P., Carlen P.L., Tator C.H. Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons. J Neurosci 1993, 13:2085-2104.
20. Manev H., Favaron M., Guidotti A., Costa E. Delayed increase of Ca2+ influx elicited by glutamate: role in neuronal death. Mol Pharmacol 1989, 36:106-112.
21. Randall R.D., Thayer S.A. Glutamate-induced calcium transient triggers delayed calcium overload and neurotoxicity in rat hippocampal neurons. J Neurosci 1992, 12:1882-1895.
22. Jordan J., Cena V., Prehn J.H. Mitochondrial control of neuron death and its role in neurodegenerative disorders. J Physiol Biochem 2003, 59:129-141.
23. Brenner C., Kroemer G. Apoptosis. Mitochondria-the death signal integrators. Science 2000, 289:1150-1151.
24. Eguchi Y., Shimizu S., Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res 1997, 57:1835-1840.
25. Gomez-Lazaro M., Galindo M.F., Concannon C.G., Segura M.F., Fernandez-Gomez F.J., Llecha N., Comella J.X., Prehn J.H., Jordan J. 6-Hydroxydopamine activates the mitochondrial apoptosis pathway through p38 MAPK-mediated, p53-independent activation of Bax and PUMA. J Neurochem 2008, 104:1599-1612.
26. Jordan J., Galindo M.F., Miller R.J. Role of calpain- and interleukin-1 beta converting enzyme-like proteases in the beta-amyloid-induced death of rat hippocampal neurons in culture. J Neurochem 1997, 68:1612-1621.
27. Lotscher H.R., Winterhalter K.H., Carafoli E., Richter C. Hydroperoxide-induced loss of pyridine nucleotides and release of calcium from rat liver mitochondria. J Biol Chem 1980, 255:9325-9330.
28. Kristal B.S., Staats P.N., Shestopalov A.I. Biochemical characterization of the mitochondrial permeability transition in isolated forebrain mitochondria. Dev Neurosci 2000, 22:376-383.
29. Sanz A., Caro P., Gomez J., Barja G. Testing the vicious cycle theory of mitochondrial ROS production: effects of H2O2 and cumene hydroperoxide treatment on heart mitochondria. J Bioenerg Biomembr 2006, 38:121-127.
30. Liu Y., Peterson D.A., Kimura H., Schubert D. Mechanism of cellular 3-(4, 5-dimethylthiazol-2-yl)-2, 5-diphenyltetrazolium bromide (MTT) reduction. J Neurochem 1997, 69:581-593.
31. Douce R., Bourguignon R., Brouquisse R., Neuberger M. Isolation of plant mitochondria: General principles and criteria of integrity. Meth Enzymol 1987, 148:403-415.
32. Garcia-Calvo M., Peterson E.P., Leiting B., Ruel R., Nicholson D.W., Thornberry N.A. Inhibition of human caspases by peptide-based and macromolecular inhibitors. J Biol Chem 1998, 273:32608-32613.
33. Reig F., Busquets M.A., Haro I., Rabanal F., Alsina M.A. Interaction of opiate molecules with lipid monolayers and liposomes. J Pharm Sci 1992, 81:546-550.
34. Gomez-Lazaro M., Galindo M.F., Fernandez-Gomez F.J., Prehn J.H., Jordan J. Activation of p53 and the pro-apoptotic p53 target gene PUMA during depolarization-induced apoptosis of chromaffin cells. Exp Neurol 2005, 196:96-103.
35. Jordan J., Galindo M.F., Tornero D., Gonzalez-Garcia C., Cena V. Bcl-x L blocks mitochondrial multiple conductance channel activation and inhibits 6-OHDA-induced death in SH-SY5Y cells. J Neurochem 2004, 89:124-133.
36. Nestler E.J. Under siege: The brain on opiates. Neuron 1996, 16:897-900.
37. Zagon I.S., McLaughlin P.J. Opioids and the apoptotic pathway in human cancer cells. Neuropeptides 2003, 37:79-88.
38. Zagon I.S., Smith J.P., Conter R., McLaughlin P.J. Identification and characterization of opioid growth factor receptor in human pancreatic adenocarcinoma. Int J Mol Med 2000, 5:77-84.
39. McLaughlin P.J., Levin R.J., Zagon I.S. Regulation of human head and neck squamous cell carcinoma growth in tissue culture by opioid growth factor. Int J Oncol 1999, 14:991-998.
40. Ren X.H., Zhao J., Pu L., Ling K., Yin D.L., Pei G. Differential neurotoxicity of etorphine-like opiates: lack of correlation with their ability to activate opiate receptors. Toxicon 1998, 36:735-743.
41. Yin D.L., Ren X.H., Zheng Z.L., Pu L., Jiang L.Z., Ma L., Pei G. Etorphine inhibits cell growth and induces apoptosis in SK-N-SH cells: involvement of pertussis toxin-sensitive G proteins. Neurosci Res 1997, 29:121-127.
42. Richter C., Schweizer M., Cossarizza A., Franceschi C. Control of apoptosis by the cellular ATP level. FEBS Lett 1996, 378:107-110.
43. Chautan M., Chazal G., Cecconi F., Gruss P., Golstein P. Interdigital cell death can occur through a necrotic and caspase-independent pathway. Curr Biol 1999, 9:967-970.
44. Marcoux F.W., Probert A.W., Weber M.L. Hypoxic neuronal injury in tissue culture is associated with delayed calcium accumulation. Stroke 1990, 21. III71-74.
45. Vergun O., Sobolevsky A.I., Yelshansky M.V., Keelan J., Khodorov B.I., Duchen M.R. Exploration of the role of reactive oxygen species in glutamate neurotoxicity in rat hippocampal neurones in culture. J Physiol 2001, 531:147-163.
46. Latta M., Kunstle G., Leist M., Wendel A. Metabolic depletion of ATP by fructose inversely controls CD95- and tumor necrosis factor receptor 1-mediated hepatic apoptosis. J Exp Med 2000, 191:1975-1985.
47. Ferrari D., Stepczynska A., Los M., Wesselborg S., Schulze-Osthoff K. Differential regulation and ATP requirement for caspase-8 and caspase-3 activation during CD95- and anticancer drug-induced apoptosis. J Exp Med 1998, 188:979-984.
48. Xiang J., Chao D.T., Korsmeyer S.J. BAX-induced cell death may not require interleukin 1 beta-converting enzyme-like proteases. Proc Natl Acad Sci USA 1996, 93:14559-14563.
49. Amarante-Mendes G.P., Finucane D.M., Martin S.J., Cotter T.G., Salvesen G.S., Green D.R. Anti-apoptotic oncogenes prevent caspase-dependent and independent commitment for cell death. Cell Death Differ 1998, 5:298-306.
50. Marsden V.S., Kaufmann T., O'Reilly A., Adams L.J.M., Strasser A. Apaf-1 and caspase-9 are required for cytokine withdrawal-induced apoptosis of mast cells but dispensable for their functional and clonogenic death. Blood 2006, 107:1872-1877.
51. Galindo M.F., Jordan J., Gonzalez-Garcia C., Cena V. Chromaffin cell death induced by 6-hydroxydopamine is independent of mitochondrial swelling and caspase activation. J Neurochem 2003, 84:1066-1073.
52. Gomez-Lazaro M., Fernandez-Gomez F.J., Jordan J. p53: twenty five years understanding the mechanism of genome protection. J Physiol Biochem 2004, 60:287-307.
53. Maneckjee R., Minna J.D. Opioids induce while nicotine suppresses apoptosis in human lung cancer cells. Cell Growth Differ 1994, 5:1033-1040.
54. Fernandez-Gomez F.J., Galindo M.F., Gomez-Lazaro M., Yuste V.J., Comella J.X., Aguirre N., Jordan J. Malonate induces cell death via mitochondrial potential collapse and delayed swelling through an ROS-dependent pathway. Br J Pharmacol 2005, 144:528-537.
55. Gottlieb E., Vander Heiden M.G., Thompson C.B. Bcl-x(L) prevents the initial decrease in mitochondrial membrane potential and subsequent reactive oxygen species production during tumor necrosis factor alpha-induced apoptosis. Mol Cell Biol 2000, 20:5680-5689.
56. McClintock D.S., Santore M.T., Lee V.Y., Brunelle J., Budinger G.R., Zong W.X., Thompson C.B., Hay N., Chandel N.S. Bcl-2 family members and functional electron transport chain regulate oxygen deprivation-induced cell death. Mol Cell Biol 2002, 22:94-104.
57. Drummer O.H., Opeskin K., Syrjanen M., Cordner S.M. Methadone toxicity causing death in ten subjects starting on a methadone maintenance program. Am J Forensic Med Pathol 1992, 13:346-350.