Phosphodiesterase 5 inhibitors prevent 3,4-methylenedioxymethamphetamine- induced 5-HT deficits in the rat

Journal of Neurochemistry

Volumn 108, Issue 3, 2009, Pages 755-766

  Puerta, Elena ^a   Hervias, Isabel ^a   Goñi Allo, Beatriz ^a   Lasheras, Berta ^a   Jordan, Joaquin ^b   Aguirre, Norberto ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

Author keywords

3,4 methylenedioxymethamphetamine; 5 hydroxytryptamine; Mitochondrial ATP sensitive K+ channels; Phosphodiesterase 5 inhibitor; Protein kinase G; Sildenafil; Vardenafil

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; 5 HYDROXYDECANOIC ACID; 8 BROMO CYCLIC GMP; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; KT 5823; PHOSPHODIESTERASE V INHIBITOR; POTASSIUM CHANNEL; PROTEIN KINASE B; SEROTONIN; SILDENAFIL; VARDENAFIL; WORTMANNIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; CORPUS STRIATUM; DRUG EFFECT; FRONTAL CORTEX; HIPPOCAMPUS; HORMONE DEFICIENCY; HYPERTHERMIA; MALE; MITOCHONDRION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SEROTONINERGIC SYSTEM; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BODY TEMPERATURE; BRAIN CHEMISTRY; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 5; HALLUCINOGENS; HYDROXYINDOLEACETIC ACID; IMIDAZOLES; KATP CHANNELS; MALE; MICROINJECTIONS; MITOCHONDRIA; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; NEOSTRIATUM; PHOSPHODIESTERASE INHIBITORS; PIPERAZINES; PURINES; RATS; RATS, WISTAR; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SIGNAL TRANSDUCTION; SULFONES; TRIAZINES;

RATTUS;

EID: 58149357087     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05825.x     Document Type: Article

References (61)

1. Abdul H. M. Butterfield D. A. (2007) Involvement of PI3K/PKG/ERK1/2 signaling pathways in cortical neurons to trigger protection by cotreatment of acetyl-l-carnitine and alpha-lipoic acid against HNE-mediated oxidative stress and neurotoxicity: implications for Alzheimer's disease. Free Radic. Biol. Med. 42, 371 384.
2. Aguirre N., Ballaz S., Lasheras B. Del Río J. (1998) MDMA ("Ecstasy") enhances 5-HT1A receptor density and 8-OH-DPAT-induced hypothermia: blockade by drugs preventing 5-hydroxytryptamine depletion. Eur. J. Pharmacol. 346, 181 188.
3. Aguirre N., Barrionuevo M., Ramírez M. J., Del Río J. Lasheras B. (1999) α-Lipoic acid prevents 3,4- methylenedioxymethamphetamine (MDMA)-induced neurotoxicity. NeuroReport 10, 3675 3680.
4. Andoh T., Chiueh C. C. Chock P. B. (2003) Cyclic GMP-dependent protein kinase regulates the expression of thioredoxin and thioredoxin peroxidase-1 during hormesis in response to oxidative stress-induced apoptosis. J. Biol. Chem. 278, 885 890.
5. Azmitia E. C. Gannon P. J. (1986) The primate serotonergic system: a review of human and animal studies and a report on Macaca fascicularis. Adv. Neurol. 43, 407 468.
6. Barrionuevo M., Aguirre N., Del Río J. Lasheras B. (2000) Serotonergic deficits and impaired passive-avoidance learning in rats by MDEA: a comparison with MDMA. Pharmacol. Biochem. Behav. 65, 233 240.
7. Burgering B. M. Coffer P. J. (1995) Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376, 599 602.
8. Commins D. L., Vosmer G., Virus R. M., Woolverton W. L., Schuster C. R. Seiden L. S. (1987) Biochemical and histological evidence that methylenedioxymethylamphetamine (MDMA) is toxic to neurons in the rat brain. J. Pharmacol. Exp. Ther. 241, 338 345.
9. Corbin J. D. Francis S. H. (1999) Cyclic GMP phosphodiesterase-5: target of sildenafil. J. Biol. Chem. 274, 13729 13732.
10. Costa A. D., Garlid K. D., West I. C., Lincoln T. M., Downey J. M., Cohen M. V. Critz S. D. (2005) Protein kinase G transmits the cardioprotective signal from cytosol to mitochondria. Circ. Res. 97, 329 336.
11. Darvesh A. S., Yamamoto B. K. Gudelsky G. A. (2005) Evidence for the involvement of nitric oxide in 3,4-methylenedioxymethamphetamine-induced serotonin depletion in the rat brain. J. Pharmacol. Exp. Ther. 312, 694 701.
12. Das A., Ockaili R., Salloum F. Kukreja R. C. (2004) Protein kinase C plays an essential role in sildenafil-induced cardioprotection in rabbits. Am. J. Physiol. Heart Circ. Physiol. 286, 1455 1460.
13. Dimmeler S., Fleming I., Fisslthaler B., Hermann C., Busse R. Zeiher A. M. (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399, 601 605.
14. Ding G., Jiang Q., Li L., Zhang L., Zhang Z. G., Ledbetter K. A., Panda S., Davarani S. P., Athiraman H., Li Q., Ewing J. R. Chopp M. (2008) Magnetic resonance imaging investigation of axonal remodeling and angiogenesis after embolic stroke in sildenafil-treated rats. J. Cereb. Blood Flow Metab. 28, 1440 1448.
15. Fulton D., Gratton J. P., McCabe T. J., Fontana J., Fujio Y., Walsh K., Franke T. F., Papapetropoulos A. Sessa W. C. (1999) Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399, 597 601.
16. Garthwaite J. Boulton C. L. (1995) Nitric oxide signaling in the central nervous system. Annu. Rev. Physiol. 57, 683 706.
17. Goñi-Allo B., Ramos M., Hervias I., Lasheras B. Aguirre N. (2006) Studies on striatal neurotoxicity caused by the 3,4- methylenedioxymethamphetamine/malonate combination: implications for serotonin/dopamine interactions. J. Psychopharmacol. 20, 245 256.
18. Goñi-Allo B., Puerta E., Hervias I., Di Palma R., Ramos M., Lasheras B. Aguirre N. (2007) Studies on the mechanisms underlying amiloride enhancement of 3,4-methylenedioxymethamphetamine-induced serotonin depletion in rats. Eur. J. Pharmacol. 562, 198 207.
19. Goñi-Allo B., O Mathúna B., Segura M., Puerta E., Lasheras B., de la Torre R. Aguirre N. (2008a) The relationship between core body temperature and 3,4-methylenedioxymethamphetamine metabolism in rats: implications for neurotoxicity. Psychopharmacology (Berl) 197, 263 278.
20. Goñi-Allo B., Puerta E., Ramos M., Lasheras B., Jordán J. Aguirre N. (2008b) Minoxidil prevents 3,4-methylenedioxymethamphetamine-induced serotonin depletions: role of mitochondrial ATP-sensitive potassium channels, Akt and ERK. J. Neurochem. 104, 914 925.
21. Green A. R., Mechan A. O., Elliott J. M., O'Shea E. Colado M. I. (2003) The pharmacology and clinical pharmacology of 3,4-methylenedioxymethamphetamine (MDMA, "ecstasy"). Pharmacol. Rev. 55, 463 508.
22. Hatzdimitrou G., McCann U. D. Ricaurte G. A. (1999) Altered serotonin innervation patterns in the forebrain of monkeys with (+/-)3,4- methylenedioxymethamphetamine seven years previously: factors influencing abnormal recovery. J. Neurosci. 19, 5096 5107.
23. Hervias I., Lasheras B. Aguirre N. (2000) 2-Deoxy-D-Glugose prevents and nicotinamide potentiates 3,4-methylenedioxymethamphetamine-induced serotonin neurotoxicity. J. Neurochem. 75, 982 990.
24. Hoyer D., Clarke D. E., Fozard J. R., Hartig P. R., Martin G. R., Mylecharane E. J., Saxena P. R. Humphrey P. P. (1994) International Union of Pharmacology classification of receptors for 5-hydroxytryptamine (Serotonin). Pharmacol. Rev. 46, 157 203.
25. Jouvert P., Revel M. O., Lazaris A., Aunis D., Langley K. Zwiller J. (2004) Activation of the cGMP pathway in dopaminergic structures reduces cocaine-induced EGR-1 expression and locomotor activity. J. Neurosci. 24, 10716 10725.
26. Kis B., Rajapakse N. C., Snipes J. A., Nagy K., Horiguchi T. Busija D. W. (2003) Diazoxide induces delayed preconditioning in cultured rat cortical neurons. J. Neurochem. 87, 969 980.
27. Kis B., Nagy K., Snipes J. A., Rajapakse N. C., Horiguchi T., Grover G. J. Busija D. W. (2004) The mitochondrial K(ATP) channel opener BMS-191095 induces neuronal preconditioning. NeuroReport 15, 345 349.
28. Kotera J., Fujishige K. Omori K. (2000) Immunohistochemical localization of cGMP-binding cGMP-specific phosphodiesterase (PDE5) in rat tissues. J. Histochem. Cytochem. 48, 685 693.
29. Kukreja R. C., Ockaili R., Salloum F., Yin C., Hawkins J., Das A. Xi L. (2004) Cardioprotection with phosphodiesterase-5 inhibition - a novel preconditioning strategy. J. Mol. Cell Cardiol. 36, 165 173.
30. Kukreja R. C., Salloum F., Das A., Ockaili R., Yin C., Bremer Y. A., Fisher P. W., Wittkamp M., Hawkins J., Chou E., Kukreja A. K., Wang X., Marwaha V. R. Xi L. (2005) Pharmacological preconditioning with sildenafil: basic mechanisms and clinical implications. Vascul. Pharmacol. 42, 219 232.
31. Lee S. Y., Andoh T., Murphy D. L. Chiueh C. C. (2003) 17Beta-estradiol activates ICI 182,780-sensitive estrogen receptors and cyclic GMP-dependent thioredoxin expression for neuroprotection. FASEB J. 17, 947 948.
32. Liu D., Lu C., Wan R., Auyeung W. W. Mattson M. P. (2002) Activation of mitochondrial ATP-dependent potassium channels protects neurons against ischemia-induced death by a mechanism involving suppression of Bax translocation and cytochrome c release. J. Cereb. Blood Flow Metab. 22, 431 443.
33. Mansergh G., Shouse R. L., Marks G., Guzman R., Rader M., Buchbinder S. Colfax G. N. (2006) Methamphetamine and sildenafil (Viagra) use are linked to unprotected receptive and insertive anal sex, respectively, in a sample of men who have sex with men. Sex Transm. Infect. 82, 131 134.
34. Mayanagi K., Gaspar T., Katakam P. V., Kis B. Busija D. W. (2007) The mitochondrial K(ATP) channel opener BMS-191095 reduces neuronal damage after transient focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 27, 348 355.
35. McCann U. D., Szabo Z., Seckin E., Rosenblatt P., Mathews W. B., Ravert H. T., Dannals R. F. Ricaurte G. A. (2005) Quantitative PET studies of the serotonin transporter in MDMA users and controls using [11C]McN5652 and [11C]DASB. Neuropsychopharmacology 30, 1741 1750.
36. Milman H. A. Arnold S. B. (2002) Neurologic, psychological, and aggressive disturbances with sildenafil. Ann. Pharmacother. 36, 1129 1134.
37. Mostafa T. (2008) Oral phosphodiesterase type 5 inhibitors: nonerectogenic beneficial uses. J. Sex Med. 5, 2502 2518.
38. Nagy K., Kis B., Rajapakse N. C., Bari F. Busija D. W. (2004) Diazoxide preconditioning protects against neuronal cell death by attenuation of oxidative stress upon glutamate stimulation. J. Neurosci. Res. 76, 697 704.
39. Obrenovitch T. P. (2008) Molecular physiology of preconditioning-induced brain tolerance to ischemia. Physiol. Rev. 88, 211 247.
40. Ockaili R., Salloum F., Hawkins J. Kukreja R. C. (2002) Sildenafil (Viagra) induces powerful cardioprotective effect via opening of mitochondrial K(ATP) channels in rabbits. Am. J. Physiol. Heart Circ. Physiol. 283, 1263 1269.
41. O'Hearn E., Battaglia G., De Souza E. B., Kuhar M. J. Molliver M. E. (1988) Methylenedioxyamphetamine (MDA) and methylenedioxymethamphetamine (MDMA) cause selective ablation of serotonergic axon terminals in forebrain: immunocytochemical evidence for neurotoxicity. J. Neurosci. 8, 2788 2803.
42. O'Shea E., Orio L., Escobedo I., Sanchez V., Camarero J., Green A. R. Colado M. I. (2006) MDMA-induced neurotoxicity: long-term effects on 5-HT biosynthesis and the influence of ambient temperature. Br. J. Pharmacol. 148, 778 785.
43. Raja S. G. (2006) Cardioprotection with sildenafil: implications for clinical practice. Curr. Med. Chem. 13, 3155 3164.
44. Ramos M., Goñi-Allo B. Aguirre N. (2004) Studies on the role of dopamine D1 receptors in the development and expression of MDMA-induced behavioral sensitization in rats. Psychopharmacology (Berl) 177, 100 110.
45. Reagan-Shaw S., Nihal M. Ahmad N. (2008) Dose translation from animal to human studies revisited. FASEB J. 22, 659 661.
46. Salloum F. N., Takenoshita Y., Ockaili R. A., Daoud V. P., Chou E., Yoshida K. Kukreja R. C. (2007) Sildenafil and vardenafil but not nitroglycerin limit myocardial infarction through opening of mitochondrial K(ATP) channels when administered at reperfusion following ischemia in rabbits. J. Mol. Cell Cardiol. 42, 453 458.
47. Sanchez V., Camarero J., Esteban B., Peter M. J., Green A. R. Colado M. I. (2001) The mechanisms involved in the long-lasting neuroprotective effect of fluoxetine against MDMA ('ecstasy')-induced degeneration of 5-HT nerve endings in rat brain. Br. J. Pharmacol. 134, 46 57.
48. Sanchez V., O'Shea E., Saadat K. S., Elliott J. M., Colado M. I. Green A. R. (2004) Effect of repeated ('binge') dosing of MDMA to rats housed at normal and high temperature on neurotoxic damage to cerebral 5-HT and dopamine neurones. J. Psychopharmacol. 18, 412 416.
49. Schlossmann J., Feil R. Hofmann F. (2003) Signaling through NO and cGMP-dependent protein kinases. Ann. Med. 35, 21 27.
50. Schmidt C. J. (1987) Neurotoxicity of the psychedelic amphetamine, methylenedioxymethamphetamine. J. Pharmacol. Exp. Ther. 240, 1 7.
51. Schmued L. C. (2003) Demonstration and localization of neuronal degeneration in the rat forebrain following a single exposure to MDMA. Brain Res. 974, 127 133.
52. Shankaran M., Yamamoto B. K. Gudelsky G. A. (1999) Involvement of the serotonin transporter in the formation of hydroxyl radicals induced by 3,4-methylenedioxymethamphetamine. Eur. J. Pharmacol. 385, 103 110.
53. Shimizu K., Lacza Z., Rajapakse N., Horiguchi T., Snipes J. Busija D. W. (2002) MitoK(ATP) opener, diazoxide, reduces neuronal damage after middle cerebral artery occlusion in the rat. Am. J. Physiol. 283, H1005 H1011.
54. Smith K. M. Romanelli F. (2005) Recreational use and misuse of phosphodiesterase 5 inhibitors. J. Am. Pharm. Assoc. 45, 63 72.
55. Sprague J. E., Banks M. L., Cook V. J. Mills E. M. (2003) Hypothalamic-pituitary-thyroid axis and sympathetic nervous system involvement in hyperthermia induced by 3,4-methylenedioxymethamphetamine (Ecstasy). J. Pharmacol. Exp. Ther. 305, 159 166.
56. Swearingen S. G. Klausner J. D. (2005) Sildenafil use, sexual risk behavior, and risk for sexually transmitted diseases, including HIV infection. Am. J. Med. 118, 571 577.
57. Teshima Y., Akao M., Li R. A., Chong T. H., Baumgartner W. A., Johnston M. V. Marban E. (2003) Mitochondrial ATP-sensitive potassium channel activation protects cerebellar granule neurons from apoptosis induced by oxidative stress. Stroke 34, 1796 1802.
58. Wang L., Gang Zhang Z., Lan Zhang R. Chopp M. (2005) Activation of the PI3-K/Akt pathway mediates cGMP enhanced-neurogenesis in the adult progenitor cells derived from the subventricular zone. J. Cereb. Blood Flow Metab. 25, 1150 1158.
59. Zhang R., Wang Y., Zhang L., Zhang Z., Tsang W., Lu M., Zhang L. Chopp M. (2002) Sildenafil (Viagra) induces neurogenesis and promotes functional recovery after stroke in rats. Stroke 33, 2675 2680.
60. Zhu C. B., Hewlett W. A., Feoktistov I., Biaggioni I. Blakely R. D. (2004a) Adenosine receptor, protein kinase G, and p38 mitogen-activated protein kinase-dependent up-regulation of serotonin transporters involves both transporter trafficking and activation. Mol. Pharmacol. 65, 1462 1474.
61. Zhu C. B., Hewlett W. A., Francis S. H., Corbin J. D. Blakely R. D. (2004b) Stimulation of serotonin transport by the cyclic GMP phosphodiesterase-5 inhibitor sildenafil. Eur. J. Pharmacol. 504, 1 6.