Clustered burst firing in FMR1 premutation hippocampal neurons: Amelioration with allopregnanolone

Human Molecular Genetics

Volumn 21, Issue 13, 2012, Pages 2923-2935

  Cao, Zhengyu ^a   Hulsizer, Susan ^a   Tassone, Flora ^a,b   Tang, Hiu Tung ^b   Hagerman, Randi J ^a,b   Rogawski, Michael A ^b   Hagerman, Paul J ^a,b   Pessah, Isaac N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID A RECEPTOR; ASPARTIC ACID DERIVATIVE; CALCIUM ION; FRAGILE X MENTAL RETARDATION PROTEIN; GLUTAMATE RECEPTOR AGONIST; IONOTROPIC RECEPTOR AGONIST; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID; PYRIDINE DERIVATIVE; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CALCIUM SIGNALING; CELL KINETICS; CONTROLLED STUDY; ELECTRODE; GENE MUTATION; HIPPOCAMPUS; IN VITRO STUDY; INTRACELLULAR SIGNALING; MALE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECORDING; WILD TYPE;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; ASPARTIC ACID; ASTROCYTES; CELLS, CULTURED; EXCITATORY AMINO ACID ANTAGONISTS; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GENE KNOCK-IN TECHNIQUES; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; N-METHYLASPARTATE; NEURONS; PREGNANOLONE; RECEPTORS, GLUTAMATE; RECEPTORS, METABOTROPIC GLUTAMATE; RNA, MESSENGER; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 84863511377     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds118     Document Type: Article

References (71)

1. Jacquemont, S., Hagerman, R.J., Hagerman, P.J. and Leehey, M.A. (2007) Fragile-X syndrome and fragile X-associated tremor/ataxia syndrome: two faces of FMR1. Lancet Neurol., 6, 45-55.
2. Hagerman, R., Au, J. and Hagerman, P. (2011) FMR1 premutation and full mutation molecular mechanisms related to autism. J. Neurodev. Disord., 3, 211-224.
3. Oostra, B.A. and Willemsen, R. (2009) FMR1: a gene with three faces. Biochim. Biophys. Acta, 1790, 467-477.
4. Brouwer, J.R., Severijnen, E., de Jong, F.H., Hessl, D., Hagerman, R.J., Oostra, B.A. and Willemsen, R. (2008) Altered hypothalamus-pituitary-adrenal gland axis regulation in the expanded CGG-repeat mouse model for fragile X-associated tremor/ataxia syndrome. Psychoneuroendocrinology, 33, 863-873.
5. Fu, Y.H., Kuhl, D.P., Pizzuti, A., Pieretti, M., Sutcliffe, J.S., Richards, S., Verkerk, A.J., Holden, J.J., Fenwick, R.G. Jr, Warren, S.T. et al. (1991) Variation of the CGG repeat at the fragile X site results in genetic instability: resolution of the Sherman paradox. Cell, 67, 1047-1058.
6. Goodlin-Jones, B.L., Tassone, F., Gane, L.W. and Hagerman, R.J. (2004) Autistic spectrum disorder and the fragile X premutation. J. Dev. Behav. Pediatr., 25, 392-398.
7. Hessl, D., Tassone, F., Loesch, D.Z., Berry-Kravis, E., Leehey, M.A., Gane, L.W., Barbato, I., Rice, C., Gould, E., Hall, D.A. et al. (2005) Abnormal elevation of FMR1 mRNA is associated with psychological symptoms in individuals with the fragile X premutation. Am. J. Med. Genet. B Neuropsychiatr. Genet., 139B, 115-121.
8. Farzin, F., Perry, H., Hessl, D., Loesch, D., Cohen, J., Bacalman, S., Gane, L., Tassone, F., Hagerman, P. and Hagerman, R. (2006) Autism spectrum disorders and attention-deficit/hyperactivity disorder in boys with the fragile X premutation. J. Dev. Behav. Pediatr., 27, S137-S144.
9. Hagerman, R.J. (2006) Lessons from fragile X regarding neurobiology, autism, and neurodegeneration. J. Dev. Behav. Pediatr., 27, 63-74.
10. Wittenberger, M.D., Hagerman, R.J., Sherman, S.L., McConkie-Rosell, A., Welt, C.K., Rebar, R.W., Corrigan, E.C., Simpson, J.L. and Nelson, L.M. (2007) The FMR1 premutation and reproduction. Fertil. Steril., 87, 456-465.
11. Amiri, K., Hagerman, R.J. and Hagerman, P.J. (2008) Fragile X-associated tremor/ataxia syndrome: an aging face of the fragile X gene. Arch. Neurol., 65, 19-25.
12. Brouwer, J.R., Willemsen, R. and Oostra, B.A. (2009) The FMR1 gene and fragile X-associated tremor/ataxia syndrome. Am. J. Med. Genet. B Neuropsychiatr. Genet., 150B, 782-798.
13. Tassone, F., Adams, J., Berry-Kravis, E.M., Cohen, S.S., Brusco, A., Leehey, M.A., Li, L., Hagerman, R.J. and Hagerman, P.J. (2007) CGG repeat length correlates with age of onset of motor signs of the fragile X-associated tremor/ataxia syndrome (FXTAS). Am. J. Med. Genet. B Neuropsychiatr. Genet., 144B, 566-569.
14. Song, F.J., Barton, P., Sleightholme, V., Yao, G.L. and Fry-Smith, A. (2003) Screening for fragile X syndrome: a literature review and modelling study. Health. Technol. Assess., 7, 1-106.
15. Hagerman, P.J. (2008) The fragile X prevalence paradox. J. Med. Genet., 45, 498-499.
16. Rodriguez-Revenga, L., Madrigal, I., Pagonabarraga, J., Xuncla, M., Badenas, C., Kulisevsky, J., Gomez, B. and Mila, M. (2009) Penetrance of FMR1 premutation associated pathologies in fragile X syndrome families. Eur. J. Hum. Genet., 17, 1359-1362.
17. Jacquemont, S., Farzin, F., Hall, D., Leehey, M., Tassone, F., Gane, L., Zhang, L., Grigsby, J., Jardini, T., Lewin, F. et al. (2004) Aging in individuals with the FMR1 mutation. Am. J. Ment. Retard., 109, 154-164.
18. Berry-Kravis, E., Abrams, L., Coffey, S.M., Hall, D.A., Greco, C., Gane, L.W., Grigsby, J., Bourgeois, J.A., Finucane, B., Jacquemont, S. et al. (2007) Fragile X-associated tremor/ataxia syndrome: clinical features, genetics, and testing guidelines. Mov. Disord., 22, 2018-2030, quiz 2140.
19. Bourgeois, J.A., Coffey, S.M., Rivera, S.M., Hessl, D., Gane, L.W., Tassone, F., Greco, C., Finucane, B., Nelson, L., Berry-Kravis, E. et al. (2009) A review of fragile X premutation disorders: expanding the psychiatric perspective. J. Clin. Psychiatry, 70, 852-862.
20. Willemsen, R., Hoogeveen-Westerveld, M., Reis, S., Holstege, J., Severijnen, L.A., Nieuwenhuizen, I.M., Schrier, M., van Unen, L., Tassone, F., Hoogeveen, A.T. et al. (2003) The FMR1 CGG repeat mouse displays ubiquitin-positive intranuclear neuronal inclusions; implications for the cerebellar tremor/ataxia syndrome. Hum. Mol. Genet., 12, 949-959.
21. Brouwer, J.R., Mientjes, E.J., Bakker, C.E., Nieuwenhuizen, I.M., Severijnen, L.A., Van der Linde, H.C., Nelson, D.L., Oostra, B.A. and Willemsen, R. (2007) Elevated Fmr1 mRNA levels and reduced protein expression in a mouse model with an unmethylated Fragile X full mutation. Exp. Cell Res., 313, 244-253.
22. Tassone, F., Hagerman, R.J., Taylor, A.K., Gane, L.W., Godfrey, T.E. and Hagerman, P.J. (2000) Elevated levels of FMR1 mRNA in carrier males: a new mechanism of involvement in the fragile-X syndrome. Am. J. Hum. Genet., 66, 6-15.
23. Greco, C.M., Hagerman, R.J., Tassone, F., Chudley, A.E., Del Bigio, M.R., Jacquemont, S., Leehey, M. and Hagerman, P.J. (2002) Neuronal intranuclear inclusions in a new cerebellar tremor/ataxia syndrome among fragile X carriers. Brain, 125, 1760-1771.
24. Greco, C.M., Berman, R.F., Martin, R.M., Tassone, F., Schwartz, P.H., Chang, A., Trapp, B.D., Iwahashi, C., Brunberg, J., Grigsby, J. et al. (2006) Neuropathology of fragile X-associated tremor/ataxia syndrome (FXTAS). Brain, 129, 243-255.
25. Tassone, F., Iwahashi, C. and Hagerman, P.J. (2004) FMR1 RNA within the intranuclear inclusions of fragile X-associated tremor/ataxia syndrome (FXTAS). RNA Biol., 1, 103-105.
26. Arocena, D.G., Iwahashi, C.K., Won, N., Beilina, A., Ludwig, A.L., Tassone, F., Schwartz, P.H. and Hagerman, P.J. (2005) Induction of inclusion formation and disruption of lamin A/C structure by premutation CGG-repeat RNA in human cultured neural cells. Hum. Mol. Genet., 14, 3661-3671.
27. Hashem, V., Galloway, J.N., Mori, M., Willemsen, R., Oostra, B.A., Paylor, R. and Nelson, D.L. (2009) Ectopic expression of CGG containing mRNA is neurotoxic in mammals. Hum. Mol. Genet., 18, 2443-2451.
28. Berman, R.F. and Willemsen, R. (2009) Mouse models of fragile x-associated tremor ataxia. J. Investig. Med., 57, 837-841.
29. Entezam, A., Biacsi, R., Orrison, B., Saha, T., Hoffman, G.E., Grabczyk, E., Nussbaum, R.L. and Usdin, K. (2007) Regional FMRP deficits and large repeat expansions into the full mutation range in a new Fragile X premutation mouse model. Gene, 395, 125-134.
30. Hunsaker, M.R., Goodrich-Hunsaker, N.J., Willemsen, R. and Berman, R.F. (2010) Temporal ordering deficits in female CGG KI mice heterozygous for the fragile X premutation. Behav. Brain Res., 213, 263-268.
31. Hunsaker, M.R., von Leden, R.E., Ta, B.T., Goodrich-Hunsaker, N.J., Arque, G., Kim, K., Willemsen, R. and Berman, R.F. (2011) Motor deficits on a ladder rung task in male and female adolescent and adult CGG knock-in mice. Behav. Brain Res., 222, 117-121.
32. Qin, M., Entezam, A., Usdin, K., Huang, T., Liu, Z.H., Hoffman, G.E. and Smith, C.B. (2011) A mouse model of the fragile X premutation: effects on behavior, dendrite morphology, and regional rates of cerebral protein synthesis. Neurobiol. Dis., 42, 85-98.
33. Hunsaker, M.R., Greco, C.M., Tassone, F., Berman, R.F., Willemsen, R., Hagerman, R.J. and Hagerman, P.J. (2011) Rare intranuclear inclusions in the brains of 3 older adult males with fragile x syndrome: implications for the spectrum of fragile x-associated disorders. J. Neuropathol. Exp. Neurol., 70, 462-469.
34. Wenzel, H.J., Hunsaker, M.R., Greco, C.M., Willemsen, R. and Berman, R.F. (2010) Ubiquitin-positive intranuclear inclusions in neuronal and glial cells in a mouse model of the fragile X premutation. Brain Res., 1318, 155-166.
35. Cunningham, C.L., Martinez Cerdeno, V., Navarro Porras, E., Prakash, A.N., Angelastro, J.M., Willemsen, R., Hagerman, P.J., Pessah, I.N., Berman, R.F. and Noctor, S.C. (2011) Premutation CGG-repeat expansion of the Fmr1 gene impairs mouse neocortical development. Hum. Mol. Genet., 20, 64-79.
36. Chen, Y., Tassone, F., Berman, R.F., Hagerman, P.J., Hagerman, R.J., Willemsen, R. and Pessah, I.N. (2010) Murine hippocampal neurons expressing Fmr1 gene premutations show early developmental deficits and late degeneration. Hum. Mol. Genet., 19, 196-208.
37. D'Hulst, C., Heulens, I., Brouwer, J.R., Willemsen, R., De Geest, N., Reeve, S.P., De Deyn, P.P., Hassan, B.A. and Kooy, R.F. (2009) Expression of the GABAergic system in animal models for fragile X syndrome and fragile X associated tremor/ataxia syndrome (FXTAS). Brain Res., 1253, 176-183.
38. Iwahashi, C., Tassone, F., Hagerman, R.J., Yasui, D., Parrott, G., Nguyen, D., Mayeur, G. and Hagerman, P.J. (2009) A quantitative ELISA assay for the fragile x mental retardation 1 protein. J. Mol. Diagn., 11, 281-289.
39. Johnstone, A.F., Gross, G.W., Weiss, D.G., Schroeder, O.H., Gramowski, A. and Shafer, T.J. (2010) Microelectrode arrays: a physiologically based neurotoxicity testing platform for the 21st century. Neurotoxicology, 31, 331-350.
40. Tanaka, T., Saito, H. and Matsuki, N. (1996) Intracellular calcium oscillation in cultured rat hippocampal neurons: a model for glutamatergic neurotransmission. Jpn J. Pharmacol., 70, 89-93.
41. Chaudhry, F.A., Reimer, R.J., Bellocchio, E.E., Danbolt, N.C., Osen, K.K., Edwards, R.H. and Storm-Mathisen, J. (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J. Neurosci., 18, 9733-9750.
42. Balschun, D., Moechars, D., Callaerts-Vegh, Z., Vermaercke, B., Van Acker, N., Andries, L. and D'Hooge, R. (2010) Vesicular glutamate transporter VGLUT1 has a role in hippocampal long-term potentiation and spatial reversal learning. Cereb. Cortex, 20, 684-693.
43. McIntire, S.L., Reimer, R.J., Schuske, K., Edwards, R.H. and Jorgensen, E.M. (1997) Identification and characterization of the vesicular GABA transporter. Nature, 389, 870-876.
44. Bellocchio, E.E., Reimer, R.J., Fremeau, R.T. Jr and Edwards, R.H. (2000) Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science, 289, 957-960.
45. Kudela, P., Franaszczuk, P.J. and Bergey, G.K. (2003) Changing excitation and inhibition in simulated neural networks: effects on induced bursting behavior. Biol. Cybern., 88, 276-285.
46. Rothstein, J.D., Dykes-Hoberg, M., Pardo, C.A., Bristol, L.A., Jin, L., Kuncl, R.W., Kanai, Y., Hediger, M.A., Wang, Y., Schielke, J.P. et al. (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron, 16, 675-686.
47. Frega, M., Pasquale, V., Tedesco, M., Marcoli, M., Contestabile, A., Nanni, M., Bonzano, L., Maura, G. and Chiappalone, M. (2012) Cortical cultures coupled to micro-electrode arrays: a novel approach to perform in vitro excitotoxicity testing. Neurotoxicol. Teratol., 34, 116-127.
48. Kokate, T.G., Svensson, B.E. and Rogawski, M.A. (1994) Anticonvulsant activity of neurosteroids: correlation with gamma-aminobutyric acid-evoked chloride current potentiation. J. Pharmacol. Exp. Ther., 270, 1223-1229.
49. Brouwer, J.R., Huizer, K., Severijnen, L.A., Hukema, R.K., Berman, R.F., Oostra, B.A. and Willemsen, R. (2008) CGG-repeat length and neuropathological and molecular correlates in a mouse model for fragile X-associated tremor/ataxia syndrome. J. Neurochem., 107, 1671-1682.
50. Hessl, D., Wang, J.M., Schneider, A., Koldewyn, K., Le, L., Iwahashi, C., Cheung, K., Tassone, F., Hagerman, P.J. and Rivera, S.M. (2011) Decreased fragile X mental retardation protein expression underlies amygdala dysfunction in carriers of the fragile X premutation. Biol. Psychiatry, 70, 859-865.
51. Chonchaiya, W., Au, J., Schneider, A., Hessl, D., Harris, S.W., Laird, M., Mu, Y., Tassone, F., Nguyen, D.V. and Hagerman, R.J. (2012) Increased prevalence of seizures in boys who were probands with the FMR1 premutation and co-morbid autism spectrum disorder. Hum. Genet., 131, 581-589.
52. 2+ transients control CNS neuronal migration. Cell Calcium, 37, 387-393.
53. Berridge, M.J. (2006) Calcium microdomains: organization and function. Cell Calcium, 40, 405-412.
54. Higley, M.J. and Sabatini, B.L. (2008) Calcium signaling in dendrites and spines: practical and functional considerations. Neuron, 59, 902-913.
55. Lohmann, C., Finski, A. and Bonhoeffer, T. (2005) Local calcium transients regulate the spontaneous motility of dendritic filopodia. Nat. Neurosci., 8, 305-312.
56. Segal, I., Korkotian, I. and Murphy, D.D. (2000) Dendritic spine formation and pruning: common cellular mechanisms? Trends Neurosci., 23, 53-57.
57. Herzog, E., Bellenchi, G.C., Gras, C., Bernard, V., Ravassard, P., Bedet, C., Gasnier, B., Giros, B. and El Mestikawy, S. (2001) The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J. Neurosci., 21, RC181.
58. Kaneko, T. and Fujiyama, F. (2002) Complementary distribution of vesicular glutamate transporters in the central nervous system. Neurosci. Res., 42, 243-250.
59. Fremeau, R.T. Jr, Kam, K., Qureshi, T., Johnson, J., Copenhagen, D.R., Storm-Mathisen, J., Chaudhry, F.A., Nicoll, R.A. and Edwards, R.H. (2004) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science, 304, 1815-1819.
60. Minelli, A., Edwards, R.H., Manzoni, T. and Conti, F. (2003) Postnatal development of the glutamate vesicular transporter VGLUT1 in rat cerebral cortex. Brain Res. Dev. Brain Res., 140, 309-314.
61. Fung, S.J., Webster, M.J. and Weickert, C.S. (2011) Expression of VGluT1 and VGAT mRNAs in human dorsolateral prefrontal cortex during development and in schizophrenia. Brain Res., 1388, 22-31.
62. Tessier, C.R. and Broadie, K. (2011) The fragile X mental retardation protein developmentally regulates the strength and fidelity of calcium signaling in Drosophila mushroom body neurons. Neurobiol. Dis., 41, 147-159.
63. Deng, P.Y., Sojka, D. and Klyachko, V.A. (2011) Abnormal presynaptic short-term plasticity and information processing in a mouse model of fragile X syndrome. J. Neurosci., 31, 10971-10982.
64. Lessard, M., Chouiali, A., Drouin, R., Sebire, G. and Corbin, F. (2012) Quantitative measurement of FMRP in blood platelets as a new screening test for fragile X syndrome. Clin. Genet., In press.
65. Gross, G.W., Rhoades, B.K., Azzazy, H.M. and Wu, M.C. (1995) The use of neuronal networks on multielectrode arrays as biosensors. Biosens. Bioelectron., 10, 553-567.
66. Keefer, E.W., Gramowski, A. and Gross, G.W. (2001) NMDA receptor-dependent periodic oscillations in cultured spinal cord networks. J. Neurophysiol., 86, 3030-3042.
67. 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. USA, 99, 7746-7750.
68. Bear, M.F., Huber, K.M. and Warren, S.T. (2004) The mGluR theory of fragile X mental retardation. Trends Neurosci., 27, 370-377.
69. Wang, L.W., Berry-Kravis, E. and Hagerman, R.J. (2010) Fragile X: leading the way for targeted treatments in autism. Neurotherapeutics, 7, 264-274.
70. Cao, Z., George, J., Baden, D.G. and Murray, T.F. (2007) Brevetoxin-induced phosphorylation of Pyk2 and Src in murine neocortical neurons involves distinct signaling pathways. Brain Res., 1184, 17-27.
71. Cao, Z., LePage, K.T., Frederick, M.O., Nicolaou, K.C. and Murray, T.F. (2010) Involvement of caspase activation in azaspiracid-induced neurotoxicity in neocortical neurons. Toxicol. Sci., 114, 323-334.