Insights into GABAAergic system deficits in fragile X syndrome lead to clinical trials

Neuropharmacology

Volumn 88, Issue , 2015, Pages 48-54

  Braat, Sien ^a   Kooy, R Frank ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Fragile X syndrome; GABAA receptor; Gaboxadol; Ganaxolone; Targeted treatment

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; FRAGILE X MENTAL RETARDATION PROTEIN; GABOXADOL; GANAXOLONE; NEUROSTEROID; NEUROTRANSMITTER; BENZODIAZEPINE RECEPTOR AFFECTING AGENT; ELTANOLONE;

AUTISM; CELL STRUCTURE; DFMR1 GENE; DISEASE COURSE; DROSOPHILA MELANOGASTER; DRUG RESEARCH; FMR1 GENE; FRAGILE X SYNDROME; GABAAERGIC SYSTEM DEFICIT; GABAERGIC SYSTEM; GENE; GENE EXPRESSION; GENETIC ASSOCIATION; HUMAN; INTELLECTUAL IMPAIRMENT; KNOCKOUT MOUSE; MUS MUSCULUS; NERVE CELL LESION; NEUROANATOMY; NEUROLOGIC DISEASE; NONHUMAN; PATHOPHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN; CLINICAL TRIAL (TOPIC); DISEASE MODEL; DRUG EFFECTS; METABOLISM; PATHOLOGY;

ANIMALS; BRAIN; CLINICAL TRIALS AS TOPIC; DISEASE MODELS, ANIMAL; FRAGILE X SYNDROME; GABA MODULATORS; HUMANS; PREGNANOLONE; RECEPTORS, GABA-A;

EID: 84908384229     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.06.028     Document Type: Review

References (50)

1. D.C. Adusei, L.K. Pacey, D. Chen, and D.R. Hampson Early developmental alterations in GABAergic protein expression in fragile X knockout mice Neuropharmacology 59 3 2010 167 171
2. M. Ascano Jr., N. Mukherjee, P. Bandaru, J.B. Miller, J.D. Nusbaum, D.L. Corcoran, C. Langlois, M. Munschauer, S. Dewell, M. Hafner, Z. Williams, U. Ohler, and T. Tuschl FMRP targets distinct mRNA sequence elements to regulate protein expression Nature 492 7429 2012 382 386
3. Y. Ben-Ari Excitatory actions of GABA during development: the nature of the nurture Nat. Rev. Neurosci. 3 9 2002 728 739
4. E. Berry-Kravis Mechanism-based treatments in neurodevelopmental disorders: fragile X syndrome Pediatr. Neurol. 50 4 2014 297 302
5. B. Bettler, and J.Y. Tiao Molecular diversity, trafficking and subcellular localization of GABAB receptors Pharmacol. Ther. 110 3 2006 533 543
6. S. Braat, and R.F. Kooy Fragile X syndrome neurobiology translates into rational therapy Drug Discov. Today 19 4 2014 510 519
7. R.B. Carter, P.L. Wood, S. Wieland, J.E. Hawkinson, D. Belelli, J.J. Lambert, H.S. White, H.H. Wolf, S. Mirsadeghi, S.H. Tahir, M.B. Bolger, N.C. Lan, and K.W. Gee Characterization of the anticonvulsant properties of ganaxolone (CCD 1042; 3alpha-hydroxy-3beta-methyl-5alpha-pregnan-20-one), a selective, high-affinity, steroid modulator of the gamma-aminobutyric acid(A) receptor J. Pharmacol. Exp. Ther. 280 3 1997 1284 1295
8. G. Cellot, and E. Cherubini Functional role of ambient GABA in refining neuronal circuits early in postnatal development Front. Neural Circuits 7 2013 136
9. D. Centonze, S. Rossi, V. Mercaldo, I. Napoli, M.T. Ciotti, V.D. Chiara, A. Musella, C. Prosperetti, P. Calabresi, G. Bernardi, and C. Bagni Abnormal striatal GABA transmission in the mouse model for the fragile X syndrome Biol. Psychiatry 63 10 2008 963 973
10. S. Chang, S.M. Bray, Z. Li, D.C. Zarnescu, C. He, P. Jin, and S.T. Warren Identification of small molecules rescuing fragile X syndrome phenotypes in Drosophila Nat. Chem. Biol. 4 4 2008 256 263
11. G. Curia, T. Papouin, P. Seguela, and M. Avoli Downregulation of tonic GABAergic inhibition in a mouse model of fragile X syndrome Cereb. Cortex 19 7 2009 1515 1520
12. M. D'Antuono, D. Merlo, and M. Avoli Involvement of cholinergic and GABAergic systems in the fragile X knockout mice Neuroscience 119 1 2003 9 13
13. C. D'Hulst, J.R. Atack, and R.F. Kooy The complexity of the GABA(A) receptor shapes unique pharmacological profiles Drug Discov. Today 14 17-18 2009 866 875
14. A receptor in fragile X syndrome Brain Res. 1121 1 2006 238 245
15. C. D'Hulst, I. Heulens, J.R. Brouwer, R. Willemsen, N. De Geest, S.P. Reeve, P.P. De Deyn, B.A. Hassan, and R.F. Kooy Expression of the GABAergic system in animal models for fragile X syndrome and fragile X associated tremor/ataxia syndrome (FXTAS) Brain Res. 1253 2009 176 183
16. C. D'Hulst, and R.F. Kooy The GABA(A) receptor: a novel target for treatment of fragile X? Trends Neurosci. 30 8 2007 425 431
17. J.C. Darnell, S.J. Van Driesche, C. Zhang, K.Y. Hung, A. Mele, C.E. Fraser, E.F. Stone, C. Chen, J.J. Fak, S.W. Chi, D.D. Licatalosi, J.D. Richter, and R.B. Darnell "FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism" Cell 146 2 2011 247 261
18. L. Davidovic, V. Navratil, C.M. Bonaccorso, M.V. Catania, B. Bardoni, and M.E. Dumas A metabolomic and systems biology perspective on the brain of the fragile X syndrome mouse model Genome Res. 2011
19. J.B. Dictenberg, S.A. Swanger, L.N. Antar, R.H. Singer, and G.J. Bassell A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome Dev. Cell 14 6 2008 926 939
20. A receptor expression in the seizure-prone fragile X mouse Neurosci. Lett. 377 3 2005 141 146
21. M. Farrant, and Z. Nusser Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors Nat. Rev. Neurosci. 6 3 2005 215 229
22. A receptor subunit d in the fragile X syndrome Neurobiol. Dis. 21 2006 346 357
23. C.L. Gatto, D. Pereira, and K. Broadie GABAergic circuit dysfunction in the drosophila fragile X syndrome model Neurobiol. Dis. 65 2014 142 159
24. J.R. Gibson, A.F. Bartley, S.A. Hays, and K.M. Huber An imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome J. Neurophysiol. 100 5 2008 2615 2626
25. M. Gruss, and K. Braun Alterations of amino acids and monoamine metabolism in male Fmr1 knockout mice: a putative animal model of the human fragile X mental retardation syndrome Neural Plast. 8 4 2001 285 298
26. R.J. Hagerman R.J. Hagerman, P.J. Hagerman, Physical and Behavioral Phenotype. Fragile X Syndrome: Diagnosis, Treatment and Research 2002 Johns Hopkins University Press Baltimore, MA 3 109
27. S. Han, C. Tai, C.J. Jones, T. Scheuer, and W.A. Catterall Enhancement of inhibitory neurotransmission by GABAA receptors having alpha2,3-subunits ameliorates behavioral deficits in a mouse model of autism Neuron 81 6 2014 1282 1289
28. Q. He, T. Nomura, J. Xu, and A. Contractor The developmental switch in GABA polarity is delayed in fragile X mice J. Neurosci. 34 2 2014 446 450
29. I. Heulens, C. D'Hulst, D. Van Dam, P.P. De Deyn, and R.F. Kooy Pharmacological treatment of fragile X syndrome with GABAergic drugs in a knockout mouse model Behav. Brain Res. 229 1 2012 244 249
30. I. Heulens, and F. Kooy Fragile X syndrome: from gene discovery to therapy Front. Biosci. 16 2011 1211 1232
31. A. Hong, A. Zhang, Y. Ke, A. El Idrissi, and C.H. Shen Downregulation of GABA(A) beta subunits is transcriptionally controlled by Fmr1p J. Mol. Neurosci. 46 2 2011 272 275
32. A.M. Hosie, K. Aronstein, D.B. Sattelle, and R.H. ffrench-Constant Molecular biology of insect neuronal GABA receptors Trends Neurosci. 20 12 1997 578 583
33. S. Kratovac, and J.G. Corbin Developmental changes in expression of inhibitory neuronal proteins in the fragile X syndrome mouse basolateral amygdala Brain Res. 1537 2013 69 78
34. 1 subtype Nat. Neurosci. 3 6 2000 587 592
35. K.Y. Miyashiro, A. Beckel-Mitchener, T.P. Purk, K.G. Becker, T. Barret, L. Liu, S. Carbonetto, I.J. Weiler, W.T. Greenough, and J. Eberwine RNA cargoes associating with FMRP reveal deficits in cellular functioning in Fmr1 null mice Neuron 37 3 2003 417 431
36. V. Nohria, and E. Giller Ganaxolone Neurotherapeutics 4 1 2007 102 105
37. J.L. Olmos-Serrano, J.G. Corbin, and M.P. Burns The GABA(A) receptor agonist THIP ameliorates specific behavioral deficits in the mouse model of fragile X syndrome Dev. Neurosci. 33 5 2011 395 403
38. J.L. Olmos-Serrano, S.M. Paluszkiewicz, B.S. Martin, W.E. Kaufmann, J.G. Corbin, and M.M. Huntsman Defective GABAergic neurotransmission and pharmacological rescue of neuronal hyperexcitability in the amygdala in a mouse model of fragile X syndrome J. Neurosci. 30 29 2010 9929 9938
39. S.M. Paluszkiewicz, J.L. Olmos-Serrano, J.G. Corbin, and M.M. Huntsman Impaired inhibitory control of cortical synchronization in fragile X syndrome J. Neurophysiol. 106 5 2011 2264 2272
40. D.S. Reddy, and M.A. Rogawski Chronic treatment with the neuroactive steroid ganaxolone in the rat induces anticonvulsant tolerance to diazepam but not to itself J. Pharmacol. Exp. Ther. 295 3 2000 Dec 1241 1248
41. D.S. Reddy, and M.A. Rogawski Neurosteroids - Endogenous Regulators of Seizure Susceptibility and Role in the Treatment of Epilepsy J.L. Noebels, M. Avoli, M.A. Rogawski, R.W. Olsen, A.V. Delgado-Escueta, SourceJasper's Basic Mechanisms of the Epilepsies [Internet] 4th ed 2012 National Center for Biotechnology Information (US) Bethesda (MD)
42. M.R. Santoro, S.M. Bray, and S.T. Warren Molecular mechanisms of fragile X syndrome: a twenty-year perspective Annu. Rev. Pathol. 7 2012 219 245
43. L. Selby, C. Zhang, and Q.-Q. Sun Major defects in neocortical GABAergic inhibitory circuits in mice lacking the fragile X mental retardation protein Neurosci. Lett. 412 3 2007 227 232
44. J.A. Suhl, P. Chopra, B.R. Anderson, G.J. Bassell, and S.T. Warren Analysis of FMRP mRNA target datasets reveals highly associated mRNAs mediated by g-quadruplex structures formed via clustered WGGA sequences Hum. Mol. Genet. 2014
45. R. Tyzio, R. Cossart, I. Khalilov, M. Minlebaev, C.A. Hubner, A. Represa, Y. Ben-Ari, and R. Khazipov Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery Science 314 5806 2006 1788 1792
46. R. Tyzio, R. Nardou, D.C. Ferrari, T. Tsintsadze, A. Shahrokhi, S. Eftekhari, I. Khalilov, V. Tsintsadze, C. Brouchoud, G. Chazal, E. Lemonnier, N. Lozovaya, N. Burnashev, and Y. Ben-Ari Oxytocin-mediated GABA inhibition during delivery attenuates autism pathogenesis in rodent offspring Science 343 6171 2014 675 679
47. A.J.M.H. Verkerk, M. Pieretti, J.S. Sutcliffe, Y.-H. Fu, D.P.A. Kuhl, A. Pizzuti, O. Reiner, S. Richards, M.F. Victoria, F. Zhang, B.E. Eussen, G.-J.B. van Ommen, L.A.J. Blonden, G.J. Riggins, J.L. Chastain, C.B. Kunst, H. Galjaard, C.T. Caskey, D.L. Nelson, B.A. Oostra, and S.T. Warren Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome Cell 65 1991 905 914
48. C.H. Vinkers, and B. Olivier Mechanisms Underlying Tolerance after Long-Term Benzodiazepine Use: A Future for Subtype-Selective GABA(A) Receptor Modulators? Adv. Pharmacol. Sci. 2012 2012 416864 10.1155/2012/416864
49. R.L. Vislay, B.S. Martin, J.L. Olmos-Serrano, S. Kratovac, D.L. Nelson, J.G. Corbin, and M.M. Huntsman Homeostatic responses fail to correct defective amygdala inhibitory circuit maturation in fragile X syndrome J. Neurosci. 33 17 2013 7548 7558
50. K.A. Wafford, and B. Ebert Gaboxadol-a new awakening in sleep Curr. Opin. Pharmacol. 6 1 2006 30 36