Novel agonists for serotonin 5-HT7 receptors reverse metabotropic glutamate receptor-mediated long-term depression in the hippocampus of wild-type and Fmr1 KO mice, a model of Fragile X Syndrome

Frontiers in Behavioral Neuroscience

Volumn 9, Issue , 2015, Pages

  Costa, Lara ^a   Sardone, Lara M ^b   Lacivita, Enza ^c   Leopoldo, Marcello ^c   Ciranna, Lucia ^b  

^a UNIVERSITY OF MESSINA   (Italy)

^b UNIVERSITY OF CATANIA   (Italy)

^c UNIVERSITY OF BARI   (Italy)

Author keywords

5 HT7; 5 HT7R agonists; Fragile X Syndrome; Hippocampus; MGluR LTD

Indexed keywords

1 (2 BIPHENYL)PIPERAZINE; 1 [2 (4 METHOXYPHENYL)PHENYL]PIPERAZINE; 1 [4 [2 (4 METHOXYPHENYL)PHENYL]PIPERAZIN 1 YL] 3 (2 PYRAZINYLOXY) 2 PROPANOL; MM 1; MM 2; N (2 FLUOROPYRIDIN 5 YLMETHYL) 4 [2 (4 METHOXY)PHENYL] 1 PIPERAZINEHEXANAMIDE,; N (4 CYANOPHENYLMETHYL) 4 (2 DIPHENYL) 1 PIPERAZINEHEXANAMIDE; SEROTONIN 7 RECEPTOR; SEROTONIN AGONIST; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DRUG HALF LIFE; DRUG STRUCTURE; FRAGILE X SYNDROME; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; IN VITRO STUDY; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; PATCH CLAMP TECHNIQUE; STRUCTURE ACTIVITY RELATION; SYNAPTIC TRANSMISSION;

EID: 84939503684     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2015.00065     Document Type: Article

References (53)

1. Adriani, W., Travaglini, D., Lacivita, E., Saso, L., Leopoldo, M., and Laviola, G. (2012). Modulatory effects of two novel agonists for serotonin receptor 7 on emotion, motivation and circadian rhythm profiles in mice.Neuropharmacology 62, 833-842. doi: 10.1016/j.neuropharm.2011.09.012
2. Bantle, J. A. (1996). Pyrimidinedione, pyrimidinetrione, triazinedione, tetrahydroquinazolinedione derivatives as alpha-1-adrenergic receptor antagonists. Eur. Pat Appl. 126, 131468.
3. Bechara, E. G., Didiot, M. C., Melko, M., Davidovic, L., Bensaid, M., Martin, P., et al. (2009). A novel function for fragile X mental retardation protein in translational activation. PLoS Biol. 7:e16. doi: 10.1371/journal.pbio.1000016
4. Bernardet, M., and Crusio, W. E. (2006). Fmr1 KO mice as a possible model of autistic features.ScientificWorldJournal 6, 1164-1176. doi: 10.1100/tsw.2006.220
5. Bhakar, A. L., Dolen, G., and Bear, M. F. (2012). The pathophysiology of fragile X (and what it teaches us about synapses). Annu. Rev. Neurosci. 35, 417-443. doi: 10.1146/annurev-neuro-060909-153138
6. Casten, K. S., Gray, A. C., and Burwell, R. D. (2011). Discrimination learning and attentional set formation in a mouse model of Fragile X. Behav. Neurosci. 125, 473-479. doi: 10.1037/a0023561
7. Choi, C. H., Schoenfeld, B. P., Bell, A. J., Hinchey, P., Kollaros, M., Gertner, M. J., et al. (2011). Pharmacological reversal of synaptic plasticity deficits in the mouse model of fragile X syndrome by group II mGluR antagonist or lithium treatment. Brain Res. 1380, 106-119. doi: 10.1016/j.brainres.2010.11.032
8. Ciranna, L., and Catania, M. V. (2014). 5-HT7 receptors as modulators of neuronal excitability, synaptic transmission and plasticity: physiological role and possible implications in autism spectrum disorders. Front. Cell Neurosci. 8:250. doi: 10.3389/fncel.2014.00250
9. Collingridge, G. L., Peineau, S., Howland, J. G., and Wang, Y. T. (2010). Long-term depression in the CNS. Nat. Rev. Neurosci. 11, 459-473. doi: 10.1038/nrn2867
10. Comery, T. A., Harris, J. B., Willems, P. J., Oostra, B. A., Irwin, S. A., Weiler, I. J., et al. (1997). Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc. Natl. Acad. Sci. U.S.A. 94, 5401-5404. doi: 10.1073/pnas.94.10.5401
11. Costa, L., Spatuzza, M., D'Antoni, S., Bonaccorso, C. M., Trovato, C., Musumeci, S. A., et al. (2012a). Activation of 5-HT7 serotonin receptors reverses metabotropic glutamate receptor-mediated synaptic plasticity in wild-type and Fmr1 knockout mice, a model of Fragile X syndrome. Biol. Psychiatry 72, 924-933. doi: 10.1016/j.biopsych.2012.06.008
12. Costa, L., Trovato, C., Musumeci, S. A., Catania, M. V., and Ciranna, L. (2012b). 5-HT1A and 5-HT7 receptors differently modulate AMPA receptor-mediated hippocampal synaptic transmission. Hippocampus 22, 790-801. doi: 10.1002/hipo.20940
13. D'Antoni, S., Spatuzza, M., Bonaccorso, C. M., Musumeci, S. A., Ciranna, L., Nicoletti, F., et al. (2014). Dysregulation of group-I metabotropic glutamate (mGlu) receptor mediated signalling in disorders associated with intellectual disability and Autism. Neurosci. Biobehav. Rev. 46(Pt 2), 228-241. doi: 10.1016/j.neubiorev.2014.02.003
14. Dolen, G., Osterweil, E., Rao, B. S., Smith, G. B., Auerbach, B. D., Chattarji, S., et al. (2007). Correction of fragile X syndrome in mice. Neuron 56, 955-962. doi: 10.1016/j.neuron.2007.12.001
15. Eriksson, T. M., Golkar, A., Ekstrom, J. C., Svenningsson, P., and Ogren, S. O. (2008). 5-HT7 receptor stimulation by 8-OH-DPAT counteracts the impairing effect of 5-HT(1A) receptor stimulation on contextual learning in mice. Eur. J. Pharmacol. 596, 107-110. doi: 10.1016/j.ejphar.2008.08.026
16. Freret, T., Paizanis, E., Beaudet, G., Gusmao-Montaigne, A., Nee, G., Dauphin, F., et al. (2014). Modulation of 5-HT7 receptor: effect on object recognition performances in mice. Psychopharmacology (Berl.) 231, 393-400. doi: 10.1007/s00213-013-3247-x
17. Garber, K. B., Visootsak, J., and Warren, S. T. (2008). Fragile X syndrome. Eur. J. Hum. Genet. 16, 666-672. doi: 10.1038/ejhg.2008.61
18. Gasbarri, A., and Pompili, A. (2014). Serotonergic 5-HT7 receptors and cognition. Rev. Neurosci. 25, 311-323. doi: 10.1515/revneuro-2013-0066
19. Hagerman, R., and Hagerman, P. (2002). Fragile X Syndrome: Diagnosis, Treatment and Research, 3rd Edn. Baltimore: John Hopkins University Press.
20. Hagerman, R. J., Ono, M. Y., and Hagerman, P. J. (2005). Recent advances in fragile X: a model for autism and neurodegeneration. Curr. Opin. Psychiatry 18, 490-496. doi: 10.1097/01.yco.0000179485.39520.b0
21. Hannon, J., and Hoyer, D. (2008). Molecular biology of 5-HT receptors. Behav. Brain Res. 195, 198-213. doi: 10.1016/j.bbr.2008.03.020
22. Hansen, H. D., Lacivita, E., Di Pilato, P., Herth, M. M., Lehel, S., Ettrup, A., et al. (2014). Synthesis, radiolabeling andin vivo evaluation of [C](R)-1-[4-[2-(4-methoxyphenyl)phenyl]piperazin-1-yl]-3-(2-pyrazinyloxy)-2-propa nol, a potential PET radioligand for the 5-HT receptor. Eur. J. Med. Chem. 79C, 152-163. doi: 10.1016/j.ejmech.2014.03.066
23. Harris, S. W., Hessl, D., Goodlin-Jones, B., Ferranti, J., Bacalman, S., Barbato, I., et al. (2008). Autism profiles of males with fragile X syndrome. Am. J. Ment. Retard. 113, 427-438. doi: 10.1352/2008.113:427-438
24. Hedlund, P. B., Leopoldo, M., Caccia, S., Sarkisyan, G., Fracasso, C., Martelli, G., et al. (2010). LP-211 is a brain penetrant selective agonist for the serotonin 5-HT(7) receptor. Neurosci. Lett. 481, 12-16. doi: 10.1016/j.neulet.2010.06.036
25. Hitchcock, S. A. (2012). Structural modifications that alter the P-glycoprotein efflux properties of compounds. J. Med. Chem. 55, 4877-4895. doi: 10.1021/jm201136z
26. Hooper, S. R., Hatton, D., Sideris, J., Sullivan, K., Hammer, J., Schaaf, J., et al. (2008). Executive functions in young males with fragile X syndrome in comparison to mental age-matched controls: baseline findings from a longitudinal study. Neuropsychology 22, 36-47. doi: 10.1037/0894-4105.22.1.36
27. Huber, K. M., Gallagher, S. M., Warren, S. T., and Bear, M. F. (2002). Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc. Natl. Acad. Sci. U.S.A. 99, 7746-7750. doi: 10.1073/pnas.122205699
28. Irwin, S. A., Galvez, R., and Greenough, W. T. (2000). Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cereb. Cortex 10, 1038-1044. doi: 10.1093/cercor/10.10.1038
29. Jia, L., and Liu, X. (2007). The conduct of drug metabolism studies considered good practice (II): in vitroexperiments. Curr. Drug Metab. 8, 822-829. doi: 10.2174/138920007782798207
30. Krueger, D. D., Osterweil, E. K., Chen, S. P., Tye, L. D., and Bear, M. F. (2011). Cognitive dysfunction and prefrontal synaptic abnormalities in a mouse model of fragile X syndrome. Proc. Natl. Acad. Sci. U.S.A. 108, 2587-2592. doi: 10.1073/pnas.1013855108
31. Lacivita, E., Niso, M., Hansen, H. D., Di Pilato, P., Herth, M. M., Lehel, S., et al. (2014). Design, synthesis, radiolabeling and in vivo evaluation of potential positron emission tomography (PET) radioligands for brain imaging of the 5-HT(7) receptor. Bioorg. Med. Chem. 22, 1736-1750. doi: 10.1016/j.bmc.2014.01.016
32. Lacivita, E., Patarnello, D., Stroth, N., Caroli, A., Niso, M., Contino, M., et al. (2012). Investigations on the 1-(2-biphenyl)piperazine motif: identification of new potent and selective ligands for the serotonin(7) (5-HT(7)) receptor with agonist or antagonist action in vitro or ex vivo. J. Med. Chem. 55, 6375-6380. doi: 10.1021/jm3003679
33. Laggerbauer, B., Ostareck, D., Keidel, E. M., Ostareck-Lederer, A., and Fischer, U. (2001). Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum. Mol. Genet. 10, 329-338. doi: 10.1093/hmg/10.4.329
34. Leopoldo, M., Lacivita, E., De Giorgio, P., Fracasso, C., Guzzetti, S., Caccia, S., et al. (2008). Structural modifications of N-(1,2,3,4-tetrahydronaphthalen-1-yl)-4-aryl-1-piperazinehexanamides: influence on lipophilicity and 5-HT7 receptor activity. Part III. J. Med. Chem. 51, 5813-5822. doi: 10.1021/jm800615e
35. Luscher, C., and Huber, K. M. (2010). Group 1 mGluR-dependent synaptic long-term depression: mechanisms and implications for circuitry and disease. Neuron 65, 445-459. doi: 10.1016/j.neuron.2010.01.016
36. Mannhold, R. (2006). "Lipophilicity: its calculation and application in ADMET predictions," in Virtual ADMET Assessment in Target Selection and Maturation, eds B. Testa and L. Turski (Amsterdam: IOS Press), 43-65.
37. Matthys, A., Haegeman, G., Van Craenenbroeck, K., and Vanhoenacker, P. (2011). Role of the 5-HT7 receptor in the central nervous system: from current status to future perspectives. Mol. Neurobiol. 43, 228-253. doi: 10.1007/s12035-011-8175-3
38. Meneses, A., Perez-Garcia, G., Liy-Salmeron, G., Ponce-Lopez, T., Lacivita, E., and Leopoldo, M. (2015). 5-HT7 receptor activation: procognitive and antiamnesic effects. Psychopharmacology (Berl.) 232, 595-603. doi: 10.1007/s00213-014-3693-0
39. Monti, J. M., Leopoldo, M., and Jantos, H. (2014). Systemic administration and local microinjection into the central nervous system of the 5-HT(7) receptor agonist LP-211 modify the sleep-wake cycle in the rat. Behav. Brain Res. 259, 321-329. doi: 10.1016/j.bbr.2013.11.030
40. Musumeci, S. A., Bosco, P., Calabrese, G., Bakker, C., De Sarro, G. B., Elia, M., et al. (2000). Audiogenic seizures susceptibility in transgenic mice with fragile X syndrome. Epilepsia 41, 19-23. doi: 10.1111/j.1528-1157.2000.tb01499.x
41. Musumeci, S. A., Ferri, R., Scuderi, C., Bosco, P., and Elia, M. (2001). Seizures and epileptiform EEG abnormalities in FRAXE syndrome. Clin. Neurophysiol. 112, 1954-1955. doi: 10.1016/S1388-2457(01)00621-6
42. Nakamoto, M., Nalavadi, V., Epstein, M. P., Narayanan, U., Bassell, G. J., and Warren, S. T. (2007). Fragile X mental retardation protein deficiency leads to excessive mGluR5-dependent internalization of AMPA receptors. Proc. Natl. Acad. Sci. U.S.A. 104, 15537-15542. doi: 10.1073/pnas.0707484104
43. Nichols, D. E., and Nichols, C. D. (2008). Serotonin receptors. Chem. Rev. 108, 1614-1641. doi: 10.1021/cr078224o
44. Nimchinsky, E. A., Oberlander, A. M., and Svoboda, K. (2001). Abnormal development of dendritic spines in FMR1 knock-out mice. J. Neurosci. 21, 5139-5146.
45. Obach, R. S., Baxter, J. G., Liston, T. E., Silber, B. M., Jones, B. C., MacIntyre, F., et al. (1997). The prediction of human pharmacokinetic parameters from preclinical and in vitro metabolism data. J. Pharmacol. Exp. Ther. 283, 46-58.
46. Osterweil, E. K., Kind, P. C., and Bear, M. F. (2012). Lifting the mood on treating fragile x. Biol. Psychiatry 72, 895-897. doi: 10.1016/j.biopsych.2012.09.017
47. Perez-Garcia, G. S., and Meneses, A. (2005). Effects of the potential 5-HT7 receptor agonist AS 19 in an autoshaping learning task. Behav. Brain Res. 163, 136-140. doi: 10.1016/j.bbr.2005.04.014
48. Pieretti, M., Zhang, F. P., Fu, Y. H., Warren, S. T., Oostra, B. A., Caskey, C. T., et al. (1991). Absence of expression of the FMR-1 gene in fragile X syndrome. Cell 66, 817-822. doi: 10.1016/0092-8674(91)90125-I
49. Sarkisyan, G., and Hedlund, P. B. (2009). The 5-HT7 receptor is involved in allocentric spatial memory information processing. Behav. Brain Res. 202, 26-31. doi: 10.1016/j.bbr.2009.03.011
50. Schmitz, D., Gloveli, T., Empson, R. M., and Heinemann, U. (1998). Comparison of the effects of serotonin in the hippocampus and the entorhinal cortex. Mol. Neurobiol. 17, 59-72. doi: 10.1007/BF02802024
51. Segal, M. (1990). Serotonin and local circuits in rat hippocampus. J. Basic Clin. Physiol. Pharmacol. 1, 77-86. doi: 10.1515/JBCPP.1990.1.1-4.77
52. Volpicelli, F., Speranza, L., di Porzio, U., Crispino, M., and Perrone-Capano, C. (2014). The serotonin receptor 7 and the structural plasticity of brain circuits. Front. Behav. Neurosci. 8:318. doi: 10.3389/fnbeh.2014.00318
53. Zhang, J., Hou, L., Klann, E., and Nelson, D. L. (2009). Altered hippocampal synaptic plasticity in the FMR1 gene family knockout mouse models. J. Neurophysiol. 101, 2572-2580. doi: 10.1152/jn.90558.2008