Regulation of postsynaptic plasticity genes' expression and topography by sustained dopamine perturbation and modulation by acute memantine: Relevance to schizophrenia

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 54, Issue , 2014, Pages 299-314

  Iasevoli, Felice ^a   Buonaguro, Elisabetta F ^a   Sarappa, Chiara ^a   Marmo, Federica ^a   Latte, Gianmarco ^a   Rossi, Rodolfo ^a   Eramo, Anna ^b   Tomasetti, Carmine ^a   de Bartolomeis, Andrea ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b LUNDBECK RESEARCH USA   (United States)

Author keywords

Antipsychotics; Homer1; NMDA receptor; PSD 95; Treatment resistant schizophrenia

Indexed keywords

8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; DOPAMINE; HALOPERIDOL; MEMANTINE; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN HOMER 1A; PROTEIN HOMER 1B; PROTEIN HOMER 1C; VANOXERINE; BENZAZEPINE DERIVATIVE; CARRIER PROTEIN; DLGH4 PROTEIN, RAT; DOPAMINE RECEPTOR BLOCKING AGENT; DOPAMINE RECEPTOR STIMULATING AGENT; DOPAMINE UPTAKE INHIBITOR; MEMBRANE PROTEIN; MESSENGER RNA; PIPERAZINE DERIVATIVE; PROTEIN HOMER; SIGNAL PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC TRANSMISSION; DRUG EFFICACY; GENE EXPRESSION; GENETIC TRANSCRIPTION; IMAGE ANALYSIS; IN SITU HYBRIDIZATION; ISOTOPE LABELING; MALE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; POSTSYNAPTIC DENSITY; POSTSYNAPTIC POTENTIAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; SCHIZOPHRENIA; SIGNAL NOISE RATIO; TOPOGRAPHY; ANIMAL; BRAIN; DRUG EFFECTS; METABOLISM; PATHOPHYSIOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ANIMALS; BENZAZEPINES; BRAIN; CARRIER PROTEINS; DOPAMINE; DOPAMINE AGENTS; DOPAMINE ANTAGONISTS; DOPAMINE UPTAKE INHIBITORS; GENE EXPRESSION; HALOPERIDOL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMANTINE; MEMBRANE PROTEINS; PIPERAZINES; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SCHIZOPHRENIA;

EID: 84904737345     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2014.07.003     Document Type: Article

References (86)

1. Abi-Dargham A., Moore H. Prefrontal DA transmission at D1 receptors and the pathology of schizophrenia. Neuroscientist 2003, 9:404-416.
2. Ambesi-Impiombato A., D'Urso G., Muscettola G., de Bartolomeis A. Method for quantitative in situ hybridization histochemistry and image analysis applied for Homer1a gene expression in rat brain. Brain Res Brain Res Protoc 2003, 11:189-196.
3. Ambesi-Impiombato A., Panariello F., Dell'aversano C., Tomasetti C., Muscettola G., de Bartolomeis A. Differential expression of Homer 1 gene by acute and chronic administration of antipsychotics and dopamine transporter inhibitors in the rat forebrain. Synapse 2007, 61:429-439.
4. Arnsten A.F. Prefrontal cortical network connections: key site of vulnerability in stress and schizophrenia. Int J Dev Neurosci 2011, 29:215-223.
5. Bamford N.S., Robinson S., Palmiter R.D., Joyce J.A., Moore C., Meshul C.K. Dopamine modulates release from corticostriatal terminals. J Neurosci 2004, 24:9541-9552.
6. Bertaso F., Roussignol G., Worley P., Bockaert J., Fagni L., Ango F. Homer1a-dependent crosstalk between NMDA and metabotropic glutamate receptors in mouse neurons. PLoS One 2010, 5:e9755.
7. Bonifati V. Genetics of Parkinson's disease - state of the art, 2013. Parkinsonism Relat Disord 2014, 20(Suppl. 1):S23-S28.
8. Borroto-Escuela D.O., Tarakanov A.O., Guidolin D., Ciruela F., Agnati L.F., Fuxe K. Moonlighting characteristics of G protein-coupled receptors: focus on receptor heteromers and relevance for neurodegeneration. IUBMB Life 2011, 63:463-472.
9. Bottai D., Guzowski J.F., Schwarz M.K., Kang S.H., Xiao B., Lanahan A., et al. Synaptic activity-induced conversion of intronic to exonic sequence in Homer 1 immediate early gene expression. J Neurosci 2002, 22:167-175.
10. Bubenikova-Valesova V., Horacek J., Vrajova M., Hoschl C. Models of schizophrenia in humans and animals based on inhibition of NMDA receptors. Neurosci Biobehav Rev 2008, 32:1014-1023.
11. Calabresi P., Maj R., Mercuri N.B., Bernardi G. Coactivation of D1 and D2 dopamine receptors is required for long-term synaptic depression in the striatum. Neurosci Lett 1992, 142:95-99.
12. Calabresi P., Mercuri N.B., Sancesario G., Bernardi G. Electrophysiology of dopamine-denervated striatal neurons. Implications for Parkinson's disease. Brain 1993, 116(Pt 2):433-452.
13. Chang H.J., Lane H.Y., Tsai G.E. NMDA pathology and treatment of schizophrenia. Curr Pharm Des 2014, DOI: CPD-EPUB-58569 and PMID: 24410561.
14. Danysz W., Parsons C.G. Alzheimer's disease, beta-amyloid, glutamate, NMDA receptors and memantine - searching for the connections. Br J Pharmacol 2012, 167:324-352.
15. de Bartolomeis A., Fiore G., Iasevoli F. Dopamine-glutamate interaction and antipsychotics mechanism of action: implication for new pharmacological strategies in psychosis. Curr Pharm Des 2005, 11:3561-3594.
16. de Bartolomeis A., Sarappa C., Magara S., Iasevoli F. Targeting glutamate system for novel antipsychotic approaches: relevance for residual psychotic symptoms and treatment resistant schizophrenia. Eur J Pharmacol 2012, 682:1-11.
17. de Bartolomeis A., Buonaguro E.F., Iasevoli F. Serotonin-glutamate and serotonin-dopamine reciprocal interactions as putative molecular targets for novel antipsychotic treatments: from receptor heterodimers to postsynaptic scaffolding and effector proteins. Psychopharmacology (Berl) 2013, 225:1-19.
18. de Bartolomeis A., Marmo F., Filomena Buonaguro E., Rossi R., Tomasetti C., Iasevoli F. Imaging brain gene expression profiles by antipsychotics: region-specific action of amisulpride on postsynaptic density transcripts compared to haloperidol. Eur Neuropsychopharmacol 2013, 23(11):1516-1529.
19. de Bartolomeis A., Sarappa C., Buonaguro E.F., Marmo F., Eramo A., Tomasetti C., et al. Different effects of the NMDA receptor antagonists ketamine, MK-801, and memantine on postsynaptic density transcripts and their topography: role of Homer signaling, and implications for novel antipsychotic and pro-cognitive targets in psychosis. Prog Neuropsychopharmacol Biol Psychiatry 2013, 46:1-12.
20. de Bartolomeis A., Latte G., Tomasetti C., Iasevoli F. Glutamatergic postsynaptic density protein dysfunctions in synaptic plasticity and dendritic spines morphology: relevance to schizophrenia and other behavioral disorders pathophysiology, and implications for novel therapeutic approaches. Mol Neurobiol 2014, 49:484-511.
21. Elkis H. Treatment-resistant schizophrenia. Psychiatr Clin North Am 2007, 30:511-533.
22. Feng W., Tu J., Pouliquin P., Cabrales E., Shen X., Dulhunty A., et al. Dynamic regulation of ryanodine receptor type 1 (RyR1) channel activity by Homer 1. Cell Calcium 2008, 43:307-314.
23. Flores-Hernandez J., Hernandez S., Snyder G.L., Yan Z., Fienberg A.A., Moss S.J., et al. D(1) dopamine receptor activation reduces GABA(A) receptor currents in neostriatal neurons through a PKA/DARPP-32/PP1 signaling cascade. J Neurophysiol 2000, 83:2996-3004.
24. Gao K., Kemp D.E., Ganocy S.J., Gajwani P., Xia G., Calabrese J.R. Antipsychotic-induced extrapyramidal side effects in bipolar disorder and schizophrenia: a systematic review. J Clin Psychopharmacol 2008, 28:203-209.
25. Gerrow K., Romorini S., Nabi S.M., Colicos M.A., Sala C., El-Husseini A. A preformed complex of postsynaptic proteins is involved in excitatory synapse development. Neuron 2006, 49:547-562.
26. Ghasemzadeh M.B., Windham L.K., Lake R.W., Acker C.J., Kalivas P.W. Cocaine activates Homer1 immediate early gene transcription in the mesocorticolimbic circuit: differential regulation by dopamine and glutamate signaling. Synapse 2009, 63:42-53.
27. Ginovart N., Kapur S. Role of dopamine D(2) receptors for antipsychotic activity. Handb Exp Pharmacol 2012, 27-52.
28. Hakansson K., Galdi S., Hendrick J., Snyder G., Greengard P., Fisone G. Regulation of phosphorylation of the GluR1 AMPA receptor by dopamine D2 receptors. J Neurochem 2006, 96:482-488.
29. Hallett P.J., Spoelgen R., Hyman B.T., Standaert D.G., Dunah A.W. Dopamine D1 activation potentiates striatal NMDA receptors by tyrosine phosphorylation-dependent subunit trafficking. J Neurosci 2006, 26:4690-4700.
30. Hashimoto K., Nakahara T., Yamada H., Hirano M., Kuroki T., Kanba S. A neurotoxic dose of methamphetamine induces gene expression of Homer 1a, but not Homer 1b or 1c, in the striatum and nucleus accumbens. Neurochem Int 2007, 51:227-232.
31. Howes O.D., Kapur S. The dopamine hypothesis of schizophrenia: version III - the final common pathway. Schizophr Bull 2009, 35:549-562.
32. Hu X.T., Wachtel S.R., Galloway M.P., White F.J. Lesions of the nigrostriatal dopamine projection increase the inhibitory effects of D1 and D2 dopamine agonists on caudate-putamen neurons and relieve D2 receptors from the necessity of D1 receptor stimulation. J Neurosci 1990, 10:2318-2329.
33. Hu J.H., Park J.M., Park S., Xiao B., Dehoff M.H., Kim S., et al. Homeostatic scaling requires group I mGluR activation mediated by Homer1a. Neuron 2010, 68:1128-1142.
34. Iasevoli F., Polese D., Ambesi-Impiombato A., Muscettola G., de Bartolomeis A. Ketamine-related expression of glutamatergic postsynaptic density genes: possible implications in psychosis. Neurosci Lett 2007, 416:1-5.
35. Iasevoli F., Tomasetti C., Ambesi-Impiombato A., Muscettola G., de Bartolomeis A. Dopamine receptor subtypes contribution to Homer1a induction: insights into antipsychotic molecular action. Prog Neuropsychopharmacol Biol Psychiatry 2009, 33:813-821.
36. Iasevoli F., Fiore G., Cicale M., Muscettola G., de Bartolomeis A. Haloperidol induces higher Homer1a expression than risperidone, olanzapine and sulpiride in striatal sub-regions. Psychiatry Res 2010, 177:255-260.
37. Iasevoli F., Tomasetti C., Marmo F., Bravi D., Arnt J., de Bartolomeis A. Divergent acute and chronic modulation of glutamatergic postsynaptic density genes expression by the antipsychotics haloperidol and sertindole. Psychopharmacology (Berl) 2010, 212:329-344.
38. Iasevoli F., Ambesi-Impiombato A., Fiore G., Panariello F., Muscettola G., de Bartolomeis A. Pattern of acute induction of Homer1a gene is preserved after chronic treatment with first- and second-generation antipsychotics: effect of short-term drug discontinuation and comparison with Homer1a-interacting genes. J Psychopharmacol 2011, 25:875-887.
39. Iasevoli F., Tomasetti C., de Bartolomeis A. Scaffolding proteins of the post-synaptic density contribute to synaptic plasticity by regulating receptor localization and distribution: relevance for neuropsychiatric diseases. Neurochem Res 2013, 38:1-22.
40. Javitt D.C., Zukin S.R., Heresco-Levy U., Umbricht D. Has an angel shown the way? Etiological and therapeutic implications of the PCP/NMDA model of schizophrenia. Schizophr Bull 2012, 38:958-966.
41. Kammermeier P.J. Endogenous Homer proteins regulate metabotropic glutamate receptor signaling in neurons. J Neurosci 2008, 28:8560-8567.
42. Kotermanski S.E., Wood J.T., Johnson J.W. Memantine binding to a superficial site on NMDA receptors contributes to partial trapping. J Physiol 2009, 587:4589-4604.
43. Li Y., Popko J., Krogh K.A., Thayer S.A. Epileptiform stimulus increases Homer 1a expression to modulate synapse number and activity in hippocampal cultures. J Neurophysiol 2013, 109:1494-1504.
44. Luo P., Li X., Fei Z., Poon W. Scaffold protein Homer 1: implications for neurological diseases. Neurochem Int 2012, 61:731-738.
45. Maekawa M., Namba T., Suzuki E., Yuasa S., Kohsaka S., Uchino S. NMDA receptor antagonist memantine promotes cell proliferation and production of mature granule neurons in the adult hippocampus. Neurosci Res 2009, 63:259-266.
46. Matsuda Y., Kishi T., Iwata N. Efficacy and safety of NMDA receptor antagonists augmentation therapy for schizophrenia: an updated meta-analysis of randomized placebo-controlled trials. J Psychiatr Res 2013, 47:2018-2020.
47. Minami I., Kengaku M., Smitt P.S., Shigemoto R., Hirano T. Long-term potentiation of mGluR1 activity by depolarization-induced Homer1a in mouse cerebellar Purkinje neurons. Eur J Neurosci 2003, 17:1023-1032.
48. Moghaddam B., Adams B., Verma A., Daly D. Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J Neurosci 1997, 17:2921-2927.
49. Nagakura A., Shitaka Y., Yarimizu J., Matsuoka N. Characterization of cognitive deficits in a transgenic mouse model of Alzheimer's disease and effects of donepezil and memantine. Eur J Pharmacol 2013, 703:53-61.
50. Papanastasiou E., Stone J.M., Shergill S. When the drugs don't work: the potential of glutamatergic antipsychotics in schizophrenia. Br J Psychiatry 2013, 202:91-93.
51. Parsons C.G., Gilling K. Memantine as an example of a fast, voltage-dependent, open channel N-methyl-d-aspartate receptor blocker. Methods Mol Biol 2007, 403:15-36.
52. Parsons C.G., Danysz W., Quack G. Memantine is a clinically well tolerated N-methyl-d-aspartate (NMDA) receptor antagonist - a review of preclinical data. Neuropharmacology 1999, 38:735-767.
53. Parsons C.G., Stoffler A., Danysz W. Memantine: a NMDA receptor antagonist that improves memory by restoration of homeostasis in the glutamatergic system - too little activation is bad, too much is even worse. Neuropharmacology 2007, 53:699-723.
54. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1997, Academic Press Inc., Sidney, Australia.
55. Pisani A., Centonze D., Bernardi G., Calabresi P. Striatal synaptic plasticity: implications for motor learning and Parkinson's disease. Mov Disord 2005, 20:395-402.
56. Remington G., Agid O., Foussias G. Schizophrenia as a disorder of too little dopamine: implications for symptoms and treatment. Expert Rev Neurother 2011, 11:589-607.
57. Ronesi J.A., Collins K.A., Hays S.A., Tsai N.P., Guo W., Birnbaum S.G., et al. Disrupted Homer scaffolds mediate abnormal mGluR5 function in a mouse model of fragile X syndrome. Nat Neurosci 2012, 15:431-440. [S1].
58. Sala C., Futai K., Yamamoto K., Worley P.F., Hayashi Y., Sheng M. Inhibition of dendritic spine morphogenesis and synaptic transmission by activity-inducible protein Homer1a. J Neurosci 2003, 23:6327-6337.
59. 2+ homeostasis at dendritic spines in hippocampal neurons. J Neurosci 2005, 25:4587-4592.
60. Samartgis J.R., Schachte L., Hazi A., Crowe S.F. Memantine facilitates memory consolidation and reconsolidation in the day-old chick. Neurobiol Learn Mem 2012, 97:380-385.
61. Sani G., Serra G., Kotzalidis G.D., Romano S., Tamorri S.M., Manfredi G., et al. The role of memantine in the treatment of psychiatric disorders other than the dementias: a review of current preclinical and clinical evidence. CNS Drugs 2012, 26:663-690.
62. Sato M., Suzuki K., Nakanishi S. NMDA receptor stimulation and brain-derived neurotrophic factor upregulate Homer 1a mRNA via the mitogen-activated protein kinase cascade in cultured cerebellar granule cells. J Neurosci 2001, 21:3797-3805.
63. Seeman P. Targeting the dopamine D2 receptor in schizophrenia. Expert Opin Ther Targets 2006, 10:515-531.
64. Shiraishi-Yamaguchi Y., Furuichi T. The Homer family proteins. Genome Biol 2007, 8:206.
65. Siddoway B., Hou H., Xia H. Molecular mechanisms of homeostatic synaptic downscaling. Neuropharmacology 2014, 78:38-44.
66. Smani T., Dionisio N., Lopez J.J., Berna-Erro A., Rosado J.A. Cytoskeletal and scaffolding proteins as structural and functional determinants of TRP channels. Biochim Biophys Acta 2014, 1838:658-664.
67. Snyder G.L., Allen P.B., Fienberg A.A., Valle C.G., Huganir R.L., Nairn A.C., et al. Regulation of phosphorylation of the GluR1 AMPA receptor in the neostriatum by dopamine and psychostimulants in vivo. J Neurosci 2000, 20:4480-4488.
68. Steiner H., Gerfen C.R. Cocaine-induced c-fos messenger RNA is inversely related to dynorphin expression in striatum. J Neurosci 1993, 13:5066-5081.
69. Tappe A., Kuner R. Regulation of motor performance and striatal function by synaptic scaffolding proteins of the Homer1 family. Proc Natl Acad Sci U S A 2006, 103:774-779.
70. Thellung S., Gatta E., Pellistri F., Corsaro A., Villa V., Vassalli M., et al. Excitotoxicity through NMDA receptors mediates cerebellar granule neuron apoptosis induced by prion protein 90-231 fragment. Neurotox Res 2013, 23:301-314.
71. Tomasetti C., Dell'Aversano C., Iasevoli F., Marmo F., de Bartolomeis A. The acute and chronic effects of combined antipsychotic-mood stabilizing treatment on the expression of cortical and striatal postsynaptic density genes. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35:184-197.
72. Tritsch N.X., Sabatini B.L. Dopaminergic modulation of synaptic transmission in cortex and striatum. Neuron 2012, 76:33-50.
73. Tu J.C., Xiao B., Yuan J.P., Lanahan A.A., Leoffert K., Li M., et al. Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 1998, 21:717-726.
74. Uramura K., Maejima Y., Shimomura K., Santoso P., Katsuda S., Kobayashi D., et al. Chronic phencyclidine treatment induces long-lasting glutamatergic activation of VTA dopamine neurons. Neurosci Lett 2014, 564:72-77.
75. Verpelli C., Schmeisser M.J., Sala C., Boeckers T.M. Scaffold proteins at the postsynaptic density. Adv Exp Med Biol 2012, 970:29-61.
76. Wei H., Dobkin C., Sheikh A.M., Malik M., Brown W.T., Li X. The therapeutic effect of memantine through the stimulation of synapse formation and dendritic spine maturation in autism and fragile X syndrome. PLoS One 2012, 7:e36981.
77. Willuhn I., Sun W., Steiner H. Topography of cocaine-induced gene regulation in the rat striatum: relationship to cortical inputs and role of behavioural context. Eur J Neurosci 2003, 17:1053-1066.
78. Xia Z., Gray J.A., Compton-Toth B.A., Roth B.L. A direct interaction of PSD-95 with 5-HT2A serotonin receptors regulates receptor trafficking and signal transduction. J Biol Chem 2003, 278:21901-21908.
79. Yamada H., Kuroki T., Nakahara T., Hashimoto K., Tsutsumi T., Hirano M., et al. The dopamine D1 receptor agonist, but not the D2 receptor agonist, induces gene expression of Homer 1a in rat striatum and nucleus accumbens. Brain Res 2007, 1131:88-96.
80. Yang L., Hong Q., Zhang M., Liu X., Pan X.Q., Guo M., et al. The role of Homer 1a in increasing locomotor activity and non-selective attention, and impairing learning and memory abilities. Brain Res 2013, 1515:39-47.
81. Yeganeh F., Nikbakht F., Bahmanpour S., Rastegar K., Namavar R. Neuroprotective effects of NMDA and group I metabotropic glutamate receptor antagonists against neurodegeneration induced by homocysteine in rat hippocampus: in vivo study. J Mol Neurosci 2013, 50:551-557.
82. Zajaczkowski W., Frankiewicz T., Parsons C.G., Danysz W. Uncompetitive NMDA receptor antagonists attenuate NMDA-induced impairment of passive avoidance learning and LTP. Neuropharmacology 1997, 36:961-971.
83. Zdanys K., Tampi R.R. A systematic review of off-label uses of memantine for psychiatric disorders. Prog Neuropsychopharmacol Biol Psychiatry 2008, 32:1362-1374.
84. Zhang G.C., Mao L.M., Liu X.Y., Parelkar N.K., Arora A., Yang L., et al. In vivo regulation of Homer1a expression in the striatum by cocaine. Mol Pharmacol 2007, 71:1148-1158.
85. Zhang J., Vinuela A., Neely M.H., Hallett P.J., Grant S.G., Miller G.M., et al. Inhibition of the dopamine D1 receptor signaling by PSD-95. J Biol Chem 2007, 282:15778-15789.
86. Zhang J., Xu T.X., Hallett P.J., Watanabe M., Grant S.G., Isacson O., et al. PSD-95 uncouples dopamine-glutamate interaction in the D1/PSD-95/NMDA receptor complex. J Neurosci 2009, 29:2948-2960.