A long hangover from party drugs: Residual proteomic changes in the hippocampus of rats 8 weeks after γ-hydroxybutyrate (GHB), 3,4-methylenedioxymethamphetamine (MDMA) or their combination

Neurochemistry International

Volumn 56, Issue 8, 2010, Pages 871-877

  van Nieuwenhuijzen, Petra S ^a   Kashem, Mohammed A ^a   Matsumoto, Izuru ^a   Hunt, Glenn E ^a   McGregor, Iain S ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

GHB; Hippocampus; MDMA; Proteomics

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; 4 HYDROXYBUTYRIC ACID; ALPHA TROPOMYOSIN; CYTOSKELETON PROTEIN; GLUTATHIONE TRANSFERASE; ONCOPROTEIN; PENTRAXIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN; TUBULIN FOLDING COFACTOR B; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CYTOSKELETON; ENVIRONMENTAL TEMPERATURE; HIPPOCAMPUS; INTRACELLULAR SIGNALING; LEARNING; LONG TERM EXPOSURE; MALE; MOLECULAR MECHANICS; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; RAT;

ANIMALS; BLOTTING, WESTERN; DRUG SYNERGISM; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HIPPOCAMPUS; MALE; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; NERVE TISSUE PROTEINS; PHARMACEUTICAL VEHICLES; PROTEOMICS; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; SODIUM OXYBATE; TIME FACTORS; UP-REGULATION;

RATTUS;

EID: 77952877837     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2010.03.002     Document Type: Article

References (65)

1. Abad M.A., Enguita M., DeGregorio-Rocasolano N., Ferrer I., Trullas R. Neuronal pentraxin 1 contributes to the neuronal damage evoked by amyloid-beta and is overexpressed in dystrophic neurites in Alzheimer's brain. J. Neurosci. 2006, 26:12735-12747.
2. Andriamampandry C., Taleb O., Viry S., Muller C., Humbert J.P., Gobaille S., Aunis D., Maitre M. Cloning and characterization of a rat brain receptor that binds the endogenous neuromodulator gamma-hydroxybutyrate (GHB). FASEB J. 2003, 17:1691-1693.
3. Arias-Cavieres A., Rozas C., Reyes-Parada M., Barrera N., Pancetti F., Loyola S., Lorca R.A., Zeise M.L., Morales B. MDMA (" ecstasy" ) impairs learning in the Morris Water Maze and reduces hippocampal LTP in young rats. Neurosci. Lett. 2009, 496:375-379.
4. Aso T., Lane W.S., Conaway J.W., Conaway R.C. Elongin (SIII): a multisubunit regulator of elongation by RNA polymerase II. Science 1995, 269:1439-1443.
5. Barszczewski M., Chua J.J., Stein A., Winter U., Heintzmann R., Zilly F.E., Fasshauer D., Lang T., Jahn R. A novel site of action for alpha-SNAP in the SNARE conformational cycle controlling membrane fusion. Mol. Biol. Cell 2008, 19:776-784.
6. Bisgaard C.F., Jayatissa M.N., Enghild J.J., Sanchez C., Artemychyn R., Wiborg O. Proteomic investigation of the ventral rat hippocampus links DRP-2 to escitalopram treatment resistance and SNAP to stress resilience in the chronic mild stress model of depression. J. Mol. Neurosci. 2007, 32:132-144.
7. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
8. Braunewell K., Riederer P., Spilker C., Gundelfinger E.D., Bogerts B., Bernstein H.G. Abnormal localization of two neuronal calcium sensor proteins, visinin-like proteins (vilips)-1 and -3, in neocortical brain areas of Alzheimer disease patients. Dement. Geriatr. Cogn. Disord. 2001, 12:110-116.
9. Camarasa J., Marimon J.M., Rodrigo T., Escubedo E., Pubill D. Memantine prevents the cognitive impairment induced by 3,4-methylenedioxymethamphetamine in rats. Eur. J. Pharmacol. 2008, 589:132-139.
10. Carter L.P., Koek W., France C.P. Behavioral analyses of GHB: receptor mechanisms. Pharmacol. Ther. 2009, 121:100-114.
11. Carter L.P., Pardi D., Gorsline J., Griffiths R.R. Illicit gamma-hydroxybutyrate (GHB) and pharmaceutical sodium oxybate (Xyrem): differences in characteristics and misuse. Drug Alcohol Depend. 2009, 104:1-10.
12. Cruz H.G., Ivanova T., Lunn M.L., Stoffel M., Slesinger P.A., Luscher C. Bi-directional effects of GABA(B) receptor agonists on the mesolimbic dopamine system. Nat. Neurosci. 2004, 7:153-159.
13. DeGregorio-Rocasolano N., Gasull T., Trullas R. Overexpression of neuronal pentraxin 1 is involved in neuronal death evoked by low K(+) in cerebellar granule cells. J. Biol. Chem. 2001, 276:796-803.
14. Einat H., Manji H.K. Cellular plasticity cascades: genes-to-behavior pathways in animal models of bipolar disorder. Biol. Psychiatry 2006, 59:1160-1171.
15. Fone K.C., Beckett S.R., Topham I.A., Swettenham J., Ball M., Maddocks L. Long-term changes in social interaction and reward following repeated MDMA administration to adolescent rats without accompanying serotonergic neurotoxicity. Psychopharmacology (Berl.) 2002, 159:437-444.
16. Fountoulakis M., Tsangaris G.T., Maris A., Lubec G. The rat brain hippocampus proteome. J. Chromatogr. B: Analyt. Technol. Biomed. Life Sci. 2005, 819:115-129.
17. Frenzilli G., Ferrucci M., Giorgi F.S., Blandini F., Nigro M., Ruggieri S., Murri L., Paparelli A., Fornai F. DNA fragmentation and oxidative stress in the hippocampal formation: a bridge between 3,4-methylenedioxymethamphetamine (ecstasy) intake and long-lasting behavioral alterations. Behav. Pharmacol. 2007, 18:471-481.
18. Fu H., Subramanian R.R., Masters S.C. 14-3-3 proteins: structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol. 2000, 40:617-647.
19. Gouzoulis-Mayfrank E., Thimm B., Rezk M., Hensen G., Daumann J. Memory impairment suggests hippocampal dysfunction in abstinent ecstasy users. Prog. Neuropsychopharmacol. Biol. Psychiatry 2003, 27:819-827.
20. Green A.R., Mechan A.O., Elliott J.M., O'Shea E., Colado M.I. The pharmacology and clinical pharmacology of 3,4-methylenedioxymethamphetamine (MDMA, " ecstasy" ). Pharmacol. Rev. 2003, 55:463-508.
21. Hargreaves G.A., Quinn H., Kashem M.A., Matsumoto I., McGregor I.S. Proteomic analysis demonstrates adolescent vulnerability to lasting hippocampal changes following chronic alcohol consumption. Alcohol. Clin. Exp. Res. 2009, 33:86-94.
22. Iwazaki T., McGregor I.S., Matsumoto I. Protein expression profile in the striatum of rats with methamphetamine-induced behavioral sensitization. Proteomics 2007, 7:1131-1139.
23. Kamura T., Burian D., Yan Q., Schmidt S.L., Lane W.S., Querido E., Branton P.E., Shilatifard A., Conaway R.C., Conaway J.W. Muf1, a novel Elongin BC-interacting leucine-rich repeat protein that can assemble with Cul5 and Rbx1 to reconstitute a ubiquitin ligase. J. Biol. Chem. 2001, 276:29748-29753.
24. 2+ signaling in the regulation of alpha-amylase expression and germination of rice seed (Oryza sativa L.). Plant Cell Physiol. 2000, 41:399-407.
25. Kaupmann K., Cryan J.F., Wellendorph P., Mombereau C., Sansig G., Klebs K., Schmutz M., Froestl W., van der Putten H., Mosbacher J., Brauner-Osborne H., Waldmeier P., Bettler B. Specific gamma-hydroxybutyrate-binding sites but loss of pharmacological effects of gamma-hydroxybutyrate in GABA(B)(1)-deficient mice. Eur. J. Neurosci. 2003, 18:2722-2730.
26. Kim H., McGrath B.M., Silverstone P.H. A review of the possible relevance of inositol and the phosphatidylinositol second messenger system (PI-cycle) to psychiatric disorders-focus on magnetic resonance spectroscopy (MRS) studies. Hum. Psychopharmacol. 2005, 20:309-326.
27. Kindlundh-Hogberg A.M., Blomqvist A., Malki R., Schioth H.B. Extensive neuroadaptive changes in cortical gene-transcript expressions of the glutamate system in response to repeated intermittent MDMA administration in adolescent rats. BMC Neurosci. 2008, 9:39.
28. Kobayashi M., Masaki T., Hori K., Masuo Y., Miyamoto M., Tsubokawa H., Noguchi H., Nomura M., Takamatsu K. Hippocalcin-deficient mice display a defect in cAMP response element-binding protein activation associated with impaired spatial and associative memory. Neuroscience 2005, 133:471-484.
29. Korhonen L., Hansson I., Kukkonen J.P., Brannvall K., Kobayashi M., Takamatsu K., Lindholm D. Hippocalcin protects against caspase-12-induced and age-dependent neuronal degeneration. Mol. Cell. Neurosci. 2005, 28:85-95.
30. Kueh D., Iwamoto K., Poling A., Baker L.E. Effects of gamma-hydroxybutyrate (GHB) and its metabolic precursors on delayed-matching-to-position performance in rats. Pharmacol. Biochem. Behav. 2008, 89:179-187.
31. Lee S.H., Choi J.H., Lee N., Lee H.R., Kim J.I., Yu N.K., Choi S.L., Kim H., Kaang B.K. Synaptic protein degradation underlies destabilization of retrieved fear memory. Science 2008, 319:1253-1256.
32. Levenson J.M., Qiu S., Weeber E.J. The role of reelin in adult synaptic function and the genetic and epigenetic regulation of the reelin gene. Biochim. Biophys. Acta 2008, 1779:422-431.
33. Li Z., Burrone J., Tyler W.J., Hartman K.N., Albeanu D.F., Murthy V.N. Synaptic vesicle recycling studied in transgenic mice expressing synaptopHluorin. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:6131-6136.
34. Lopez-Fanarraga M., Carranza G., Bellido J., Kortazar D., Villegas J.C., Zabala J.C. Tubulin cofactor B plays a role in the neuronal growth cone. J. Neurochem. 2007, 100:1680-1687.
35. Maitre M. The gamma-hydroxybutyrate signalling system in brain: organization and functional implications. Prog. Neurobiol. 1997, 51:337-361.
36. Matsuda-Matsumoto H., Iwazaki T., Kashem M.A., Harper C., Matsumoto I. Differential protein expression profiles in the hippocampus of human alcoholics. Neurochem. Int. 2007, 51:370-376.
37. Matsuki T., Pramatarova A., Howell B.W. Reduction of Crk and CrkL expression blocks reelin-induced dendritogenesis. J. Cell Sci. 2008, 121:1869-1875.
38. McGregor I.S., Callaghan P.D., Hunt G.E. From ultrasocial to antisocial: a role for oxytocin in the acute reinforcing effects and long-term adverse consequences of drug use?. Br. J. Pharmacol. 2008, 154:358-368.
39. McGregor I.S., Clemens K.J., Van der Plasse G., Li K.M., Hunt G.E., Chen F., Lawrence A.J. Increased anxiety 3 months after brief exposure to MDMA (" Ecstasy" ) in rats: association with altered 5-HT transporter and receptor density. Neuropsychopharmacology 2003, 28:1472-1484.
40. McGregor I.S., Gurtman C.G., Morley K.C., Clemens K.J., Blokland A., Li K.M., Cornish J.L., Hunt G.E. Increased anxiety and " depressive" symptoms months after MDMA (" ecstasy" ) in rats: drug-induced hyperthermia does not predict long-term outcomes. Psychopharmacology (Berl.) 2003, 168:465-474.
41. Pacchioni A.M., Vallone J., Worley P., Kalivas P.W. Neuronal pentraxins modulate cocaine-induced neuroadaptations. J. Pharmacol. Exp. Ther. 2009, 328:183-192.
42. Park T.J., Curran T. Crk and Crk-like play essential overlapping roles downstream of disabled-1 in the Reelin pathway. J. Neurosci. 2008, 28:13551-13562.
43. Pedraza C., Garcia F.B., Navarro J.F. Neurotoxic effects induced by gammahydroxybutyric acid (GHB) in male rats. Int. J. Neuropsychopharmacol. 2009, 12:1165-1177.
44. Piper B.J., Fraiman J.B., Owens C.B., Ali S.F., Meyer J.S. Dissociation of the neurochemical and behavioral toxicology of MDMA ('Ecstasy') by citalopram. Neuropsychopharmacology 2008, 33:1192-1205.
45. Quinn H.R., Matsumoto I., Callaghan P.D., Long L.E., Arnold J.C., Gunasekaran N., Thompson M.R., Dawson B., Mallet P.E., Kashem M.A., Matsuda-Matsumoto H., Iwazaki T., McGregor I.S. Adolescent rats find repeated delta(9)-THC less aversive than adult rats but display greater residual cognitive deficits and changes in hippocampal protein expression following exposure. Neuropsychopharmacology 2008, 33:1113-1126.
46. Ramos J.W. The regulation of extracellular signal-regulated kinase (ERK) in mammalian cells. Int. J. Biochem. Cell Biol. 2008, 40:2707-2719.
47. Renault F., Formstecher E., Callebaut I., Junier M.P., Chneiweiss H. The multifunctional protein PEA-15 is involved in the control of apoptosis and cell cycle in astrocytes. Biochem. Pharmacol. 2003, 66:1581-1588.
48. Ryu M.J., Kim D., Kang U.B., Kim J., Shin H.S., Lee C., Yu M.H. Proteomic analysis of gamma-butyrolactone-treated mouse thalamus reveals dysregulated proteins upon absence seizure. J. Neurochem. 2007, 102:646-656.
49. Sgaravatti A.M., Magnusson A.S., Oliveira A.S., Mescka C.P., Zanin F., Sgarbi M.B., Pederzolli C.D., Wyse A.T., Wannmacher C.M., Wajner M., Dutra-Filho C.S. Effects of 1,4-butanediol administration on oxidative stress in rat brain: study of the neurotoxicity of gamma-hydroxybutyric acid in vivo. Metab. Brain Dis. 2009, 24:271-282.
50. Sircar R., Basak A. Adolescent gamma-hydroxybutyric acid exposure decreases cortical N-methyl-d-aspartate receptor and impairs spatial learning. Pharmacol. Biochem. Behav. 2004, 79:701-708.
51. Sircar R., Basak A., Sircar D. Gamma-hydroxybutyric acid-induced cognitive deficits in the female adolescent rat. Ann. N.Y. Acad. Sci. 2008, 1139:386-389.
52. Storey J.D., Tibshirani R. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:9440-9445.
53. Sumnall H.R., Woolfall K., Edwards S., Cole J.C., Beynon C.M. Use, function, and subjective experiences of gamma-hydroxybutyrate (GHB). Drug Alcohol Depend. 2008, 92:286-290.
54. Tchaikovskaya T., Fraifeld V., Urphanishvili T., Andorfer J.H., Davies P., Listowsky I. Glutathione S-transferase hGSTM3 and ageing-associated neurodegeneration: relationship to Alzheimer's disease. Mech. Ageing Dev. 2005, 126:309-315.
55. Thiriet N., Ladenheim B., McCoy M.T., Cadet J.L. Analysis of ecstasy (MDMA)-induced transcriptional responses in the rat cortex. FASEB J. 2002, 16:1887-1894.
56. Toyo-oka K., Shionoya A., Gambello M.J., Cardoso C., Leventer R., Ward H.L., Ayala R., Tsai L.H., Dobyns W., Ledbetter D., Hirotsune S., Wynshaw-Boris A. 14-3-3epsilon is important for neuronal migration by binding to NUDEL: a molecular explanation for Miller-Dieker syndrome. Nat. Genet. 2003, 34:274-285.
57. Uys J.D., Niesink R.J. Pharmacological aspects of the combined use of 3,4-methylenedioxymethamphetamine (MDMA, ecstasy) and gamma-hydroxybutyric acid (GHB): a review of the literature. Drug Alcohol Rev. 2005, 24:359-368.
58. van Nieuwenhuijzen P.S., Li K., Hunt G.E., McGregor I.S. Weekly gamma-hydroxybutyrate (GHB) exposure sensitizes locomotor hyperactivity to low dose 3,4-methylenedioxymethamphetamine (MDMA) in rats. Neuropsychobiology 2009, 60:195-203.
59. van Nieuwenhuijzen, P.S., Long, L.E., Hunt, G.E., Arnold, J.C., McGregor, I.S. submitted for publication. Residual social, memory and oxytocin-related changes in rats following repeated exposure to γ-hydroxybutyrate (GHB), 3,4-methylenedioxymethamphetamine (MDMA) or their combination.
60. van Nieuwenhuijzen P.S., McGregor I.S., Hunt G.E. The distribution of gamma-hydroxybutyrate-induced Fos expression in rat brain: comparison with baclofen. Neuroscience 2009, 158:441-455.
61. Vorhees C.V., Schaefer T.L., Skelton M.R., Grace C.E., Herring N.R., Williams M.T. (+/-)3,4-Methylenedioxymethamphetamine (MDMA) dose-dependently impairs spatial learning in the morris water maze after exposure of rats to different five-day intervals from birth to postnatal day twenty. Dev. Neurosci. 2009, 31:107-120.
62. Wang T., Zhang W., Pei Z., Block M., Wilson B., Reece J.M., Miller D.S., Hong J.S. Reactive microgliosis participates in MPP+-induced dopaminergic neurodegeneration: role of 67kDa laminin receptor. FASEB J. 2006, 20:906-915.
63. +-ATPase in brain synaptic vesicles at micromolar concentrations. J. Neurochem. 1998, 70:646-652.
64. Wilkens S., Zhang Z., Zheng Y. A structural model of the vacuolar ATPase from transmission electron microscopy. Micron 2005, 36:109-126.
65. Zhang M., Moon C., Chan G.C., Yang L., Zheng F., Conti A.C., Muglia L., Muglia L.J., Storm D.R., Wang H. Ca-stimulated type 8 adenylyl cyclase is required for rapid acquisition of novel spatial information and for working/episodic-like memory. J. Neurosci. 2008, 28:4736-4744.