Re-arrangements of gene transcripts at glutamatergic synapses after prolonged treatments with antipsychotics: A putative link with synaptic remodeling

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 76, Issue , 2017, Pages 29-41

  Buonaguro, Elisabetta Filomena ^a   Iasevoli, Felice ^a   Marmo, Federica ^a   Eramo, Anna ^b   Latte, Gianmarco ^a   Avagliano, Camilla ^a   Tomasetti, Carmine ^a   de Bartolomeis, Andrea ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b LUNDBECK RESEARCH USA   (United States)

Author keywords

Atypical antipsychotic; Brain imaging; PSD 95; Schizophrenia; Shank

Indexed keywords

ASENAPINE; HALOPERIDOL; OLANZAPINE; BENZODIAZEPINE DERIVATIVE; DISKS LARGE HOMOLOG 4; DLG4 PROTEIN, RAT; FUSED HETEROCYCLIC RINGS; NERVE PROTEIN; NEUROLEPTIC AGENT; SHANK1 PROTEIN, RAT;

ANIMAL EXPERIMENT; ARC GENE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; GENE; GENE EXPRESSION; GENE REARRANGEMENT; GENETIC TRANSCRIPTION; GLUTAMATERGIC SYNAPSE; HOMER1A GENE; INSULA; MALE; MOLECULAR IMAGING; MOTOR CORTEX; NONHUMAN; NUCLEUS ACCUMBENS; POSTSYNAPTIC DENSITY; PSD 95 GENE; RAT; SCHIZOPHRENIA; SHANK1 GENE; SOMATOSENSORY CORTEX; ANIMAL; BRAIN CORTEX; DRUG EFFECTS; NEOSTRIATUM; NERVE CELL PLASTICITY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIPSYCHOTIC AGENTS; BENZODIAZEPINES; CEREBRAL CORTEX; DISKS LARGE HOMOLOG 4 PROTEIN; GENE EXPRESSION; HALOPERIDOL; HETEROCYCLIC COMPOUNDS, 4 OR MORE RINGS; MALE; NEOSTRIATUM; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; POST-SYNAPTIC DENSITY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 85014026928     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2017.02.012     Document Type: Article

References (57)

1. 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. 11 (2003), 189–196.
2. Ango, F., Prezeau, L., Muller, T., Tu, J.C., Xiao, B., Worley, P.F., et al. Agonist-independent activation of metabotropic glutamate receptors by the intracellular protein Homer. Nature 411 (2001), 962–965.
3. 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, 5, 2010, e9755.
4. Bramham, C.R., Worley, P.F., Moore, M.J., Guzowski, J.F., The immediate early gene arc/arg3.1: regulation, mechanisms, and function. J. Neurosci. 28 (2008), 11760–11767.
5. Buonaguro, E.F., Tomasetti, C., Chiodini, P., Marmo, F., Latte, G., Rossi, R., et al. Postsynaptic density protein transcripts are differentially modulated by minocycline alone or in add-on to haloperidol: Implications for treatment resistant schizophrenia. J. Psychopharmacol., 2016.
6. Bymaster, F.P., Hemrick-Luecke, S.K., Perry, K.W., Fuller, R.W., Neurochemical evidence for antagonism by olanzapine of dopamine, serotonin, alpha 1-adrenergic and muscarinic receptors in vivo in rats. Psychopharmacology 124 (1996), 87–94.
7. Chen, X., Levy, J.M., Hou, A., Winters, C., Azzam, R., Sousa, A.A., et al. PSD-95 family MAGUKs are essential for anchoring AMPA and NMDA receptor complexes at the postsynaptic density. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), E6983–E6992.
8. Correll, C.U., From receptor pharmacology to improved outcomes: individualising the selection, dosing, and switching of antipsychotics. Eur. Psychiatry 25:Suppl. 2 (2010), S12–S21.
9. de Bartolomeis, A., Iasevoli, F., The Homer family and the signal transduction system at glutamatergic postsynaptic density: potential role in behavior and pharmacotherapy. Psychopharmacol. Bull. 37 (2003), 51–83.
10. de Bartolomeis, A., Iasevoli, F., Marmo, F., Buonaguro, E.F., Eramo, A., Rossi, R., et al. Progressive recruitment of cortical and striatal regions by inducible postsynaptic density transcripts after increasing doses of antipsychotics with different receptor profiles: insights for psychosis treatment. Eur. Neuropsychopharmacol. 25 (2015), 566–582.
11. 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. 49 (2014), 484–511.
12. de Bartolomeis, A., Marmo, F., Buonaguro, E.F., Latte, G., Tomasetti, C., Iasevoli, F., Switching antipsychotics: imaging the differential effect on the topography of postsynaptic density transcripts in antipsychotic-naive vs. antipsychotic-exposed rats. Prog. Neuropsychopharmacol. Biol. Psychiatry 70 (2016), 24–38.
13. de Bartolomeis, A., Marmo, F., Buonaguro, E.F., 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. 23 (2013), 1516–1529.
14. 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. Neuro-Psychopharmacol. Biol. Psychiatry 46 (2013), 1–12.
15. Dean, B., Thomas, N., Lai, C.Y., Chen, W.J., Scarr, E., Changes in cholinergic and glutamatergic markers in the striatum from a sub-set of subjects with schizophrenia. Schizophr. Res. 169 (2015), 83–88.
16. Dosemeci, A., Makusky, A.J., Jankowska-Stephens, E., Yang, X., Slotta, D.J., Markey, S.P., Composition of the synaptic PSD-95 complex. Mol. Cell. Proteomics 6 (2007), 1749–1760.
17. Fromer, M., Pocklington, A.J., Kavanagh, D.H., Williams, H.J., Dwyer, S., Gormley, P., et al. De novo mutations in schizophrenia implicate synaptic networks. Nature 506 (2014), 179–184.
18. Fumagalli, F., Frasca, A., Racagni, G., Riva, M.A., Dynamic regulation of glutamatergic postsynaptic activity in rat prefrontal cortex by repeated administration of antipsychotic drugs. Mol. Pharmacol. 73 (2008), 1484–1490.
19. Gao, C., Tronson, N.C., Radulovic, J., Modulation of behavior by scaffolding proteins of the post-synaptic density. Neurobiol. Learn. Mem. 105 (2013), 3–12.
20. Guzowski, J.F., Lyford, G.L., Stevenson, G.D., Houston, F.P., McGaugh, J.L., Worley, P.F., et al. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J. Neurosci. 20 (2000), 3993–4001.
21. Hall, J., Trent, S., Thomas, K.L., O'Donovan, M.C., Owen, M.J., Genetic risk for schizophrenia: convergence on synaptic pathways involved in plasticity. Biol. Psychiatry 77 (2015), 52–58.
22. Ho, B.C., Andreasen, N.C., Ziebell, S., Pierson, R., Magnotta, V., Long-term antipsychotic treatment and brain volumes: a longitudinal study of first-episode schizophrenia. Arch. Gen. Psychiatry 68 (2011), 128–137.
23. Huang, M., Li, Z., Dai, J., Shahid, M., Wong, E.H., Meltzer, H.Y., Asenapine increases dopamine, norepinephrine, and acetylcholine efflux in the rat medial prefrontal cortex and hippocampus. Neuropsychopharmacology 33 (2008), 2934–2945.
24. Hwang, J.I., Kim, H.S., Lee, J.R., Kim, E., Ryu, S.H., Suh, P.G., The interaction of phospholipase C-beta3 with Shank2 regulates mGluR-mediated calcium signal. J. Biol. Chem. 280 (2005), 12467–12473.
25. 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. 25 (2011), 875–887.
26. 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. 177 (2010), 255–260.
27. 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. Neuro-Psychopharmacol. Biol. Psychiatry 33 (2009), 813–821.
28. Iasevoli, F., Tomasetti, C., Buonaguro, E.F., de Bartolomeis, A., The glutamatergic aspects of schizophrenia molecular pathophysiology: role of the postsynaptic density, and implications for treatment. Curr. Neuropharmacol. 12 (2014), 219–238.
29. 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. 38 (2013), 1–22.
30. Kammermeier, P.J., Endogenous homer proteins regulate metabotropic glutamate receptor signaling in neurons. J. Neurosci. 28 (2008), 8560–8567.
31. Kontkanen, O., Toronen, P., Lakso, M., Wong, G., Castren, E., Antipsychotic drug treatment induces differential gene expression in the rat cortex. J. Neurochem. 83 (2002), 1043–1053.
32. Kumar, V., Fahey, P.G., Jong, Y.J., Ramanan, N., O'Malley, K.L., Activation of intracellular metabotropic glutamate receptor 5 in striatal neurons leads to up-regulation of genes associated with sustained synaptic transmission including Arc/Arg3.1 protein. J. Biol. Chem. 287 (2012), 5412–5425.
33. Li, Y., Pehrson, A.L., Waller, J.A., Dale, E., Sanchez, C., Gulinello, M., A critical evaluation of the activity-regulated cytoskeleton-associated protein (Arc/Arg3.1)'s putative role in regulating dendritic plasticity, cognitive processes, and mood in animal models of depression. Front. Neurosci., 9, 2015, 279.
34. Marston, H.M., Young, J.W., Martin, F.D., Serpa, K.A., Moore, C.L., Wong, E.H., et al. Asenapine effects in animal models of psychosis and cognitive function. Psychopharmacology 206 (2009), 699–714.
35. Murakoshi, H., Yasuda, R., Postsynaptic signaling during plasticity of dendritic spines. Trends Neurosci. 35 (2012), 135–143.
36. Newell, K.A., Matosin, N., Rethinking metabotropic glutamate receptor 5 pathological findings in psychiatric disorders: implications for the future of novel therapeutics. BMC Psychiatry, 14, 2014, 23.
37. Park, S., Park, J.M., Kim, S., Kim, J.A., Shepherd, J.D., Smith-Hicks, C.L., et al. Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of Arc/Arg3.1 essential for mGluR-LTD. Neuron 59 (2008), 70–83.
38. Paxinos, G., Watson, C., The rat brain. Stereotaxic Coordinates, sixth ed., 2007, Academic Press Inc., Sidney, Australia.
39. Purcell, S.M., Moran, J.L., Fromer, M., Ruderfer, D., Solovieff, N., Roussos, P., et al. A polygenic burden of rare disruptive mutations in schizophrenia. Nature 506 (2014), 185–190.
40. Sala, C., Roussignol, G., Meldolesi, J., Fagni, L., Key role of the postsynaptic density scaffold proteins Shank and Homer in the functional architecture of Ca2 + homeostasis at dendritic spines in hippocampal neurons. J. Neurosci. 25 (2005), 4587–4592.
41. Sala, C., Vicidomini, C., Bigi, I., Mossa, A., Verpelli, C., Shank synaptic scaffold proteins: keys to understanding the pathogenesis of autism and other synaptic disorders. J. Neurochem. 135 (2015), 849–858.
42. Scheidemantel, T., Korobkova, I., Rej, S., Sajatovic, M., Asenapine for bipolar disorder. Neuropsychiatr. Dis. Treat. 11 (2015), 3007–3017.
43. Serchov, T., Clement, H.W., Schwarz, M.K., Iasevoli, F., Tosh, D.K., Idzko, M., et al. Increased signaling via adenosine A1 receptors, sleep deprivation, imipramine, and ketamine inhibit depressive-like behavior via induction of Homer1a. Neuron 87 (2015), 549–562.
44. Shahid, M., Walker, G.B., Zorn, S.H., Wong, E.H., Asenapine: a novel psychopharmacologic agent with a unique human receptor signature. J. Psychopharmacol. 23 (2009), 65–73.
45. Shiraishi-Yamaguchi, Y., Furuichi, T., The Homer family proteins. Genome Biol., 8, 2007, 206.
46. Siddoway, B., Hou, H., Xia, H., Molecular mechanisms of homeostatic synaptic downscaling. Neuropharmacology 78 (2014), 38–44.
47. Steiner, H., Gerfen, C.R., Cocaine-induced c-fos messenger RNA is inversely related to dynorphin expression in striatum. J. Neurosci. 13 (1993), 5066–5081.
48. Tarazi, F.I., Stahl, S.M., Iloperidone, asenapine and lurasidone: a primer on their current status. Expert. Opin. Pharmacother. 13 (2012), 1911–1922.
49. Tomasetti, C., Dell'Aversano, C., Iasevoli, F., de Bartolomeis, A., Homer splice variants modulation within cortico-subcortical regions by dopamine D2 antagonists, a partial agonist, and an indirect agonist: implication for glutamatergic postsynaptic density in antipsychotics action. Neuroscience 150 (2007), 144–158.
50. Tu, J.C., Xiao, B., Naisbitt, S., Yuan, J.P., Petralia, R.S., Brakeman, P., et al. Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 23 (1999), 583–592.
51. Verpelli, C., Schmeisser, M.J., Sala, C., Boeckers, T.M., Scaffold proteins at the postsynaptic density. Adv. Exp. Med. Biol. 970 (2012), 29–61.
52. Vita, A., De Peri, L., Deste, G., Barlati, S., Sacchetti, E., The effect of antipsychotic treatment on cortical gray matter changes in schizophrenia: does the class matter? A meta-analysis and meta-regression of longitudinal magnetic resonance imaging studies. Biol. Psychiatry 78 (2015), 403–412.
53. Wagner, K.V., Hartmann, J., Labermaier, C., Hausl, A.S., Zhao, G., Harbich, D., et al. Homer1/mGluR5 activity moderates vulnerability to chronic social stress. Neuropsychopharmacology 40 (2015), 1222–1233.
54. Wang, Y., Rao, W., Zhang, C., Zhang, C., Liu, M.D., Han, F., et al. Scaffolding protein Homer1a protects against NMDA-induced neuronal injury. Cell Death Dis., 6, 2015, e1843.
55. 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. 17 (2003), 1053–1066.
56. Xiberas, X., Martinot, J.L., Mallet, L., Artiges, E., Loc, H.C., Maziere, B., et al. Extrastriatal and striatal D(2) dopamine receptor blockade with haloperidol or new antipsychotic drugs in patients with schizophrenia. Br. J. Psychiatry 179 (2001), 503–508.
57. Zhang, P., Lisman, J.E., Activity-dependent regulation of synaptic strength by PSD-95 in CA1 neurons. J. Neurophysiol. 107 (2012), 1058–1066.