Imbalance of excitatory/inhibitory synaptic protein expression in iPSC-derived neurons from FOXG1 patients and in foxg1 mice

European Journal of Human Genetics

Volumn 24, Issue 6, 2016, Pages 871-880

  Patriarchi, Tommaso ^a,b   Amabile, Sonia ^a   Frullanti, Elisa ^c   Landucci, Elisa ^a   Lo Rizzo, Caterina ^a   Ariani, Francesca ^a,c   Costa, Mario ^d,e   Olimpico, Francesco ^d   Hell, Johannes W ^b   Vaccarino, Flora M ^f,g   Renieri, Alessandra ^a,c   Meloni, Ilaria ^a  

^a UNIVERSITY OF SIENA   (Italy)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY HOSPITAL OF SIENA   (Italy)

^d CNR   (Italy)

^e SCUOLA NORMALE SUPERIORE   (Italy)

^f YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; AMPA RECEPTOR; BIOLOGICAL MARKER; EXCITATORY SYNAPTIC PROTEIN; GLUTAMATE DECARBOXYLASE 67; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR A1; GLUTAMATE RECEPTOR DELTA 1; INHIBITORY SYNAPTIC PROTEIN; MESSENGER RNA; NERVE PROTEIN; NMDA TYPE RECEPTOR SUBUNIT GLUN1; POSTSYNAPTIC DENSITY PROTEIN 95; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2; FORKHEAD TRANSCRIPTION FACTOR; FOXG1 PROTEIN, HUMAN; FOXG1 PROTEIN, MOUSE; GLUD1 PROTEIN, HUMAN; GLUD1 PROTEIN, MOUSE; GLUTAMATE DEHYDROGENASE;

ADULT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CDKL5 GENE; CONTROLLED STUDY; DISEASE SEVERITY; EMBRYO; EMBRYO DEVELOPMENT; FETUS; FOXG1 GENE; GABAERGIC SYSTEM; GENE; GENE MUTATION; GENETIC MARKER; HUMAN; HUMAN CELL; INDUCED PLURIPOTENT STEM CELL; MECP2 GENE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RETT SYNDROME; RNA ANALYSIS; ADOLESCENT; ANIMAL; BRAIN; C57BL MOUSE; CELL CULTURE; CYTOLOGY; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; INFANT; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; SYNAPSE;

ADOLESCENT; ANIMALS; BRAIN; CELLS, CULTURED; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GLUTAMATE DEHYDROGENASE; HUMANS; INDUCED PLURIPOTENT STEM CELLS; INFANT; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; RECEPTORS, GLUTAMATE; RETT SYNDROME; SYNAPSES;

EID: 84943339642     PISSN: 10184813     EISSN: 14765438     Source Type: Journal    
DOI: 10.1038/ejhg.2015.216     Document Type: Article

References (58)

1. Chahrour M, Zoghbi HY. The story of Rett syndrome: from clinic to neurobiology. Neuron 2007; 56: 422-437
2. Ariani F, Hayek G, Rondinella D, et al. FOXG1 is responsible for the congenital variant of Rett syndrome. Am J Hum Genet 2008; 83: 89-93
3. Bertani I, Rusconi L, Bolognese F, et al. Functional consequences of mutations in CDKL5, an X-linked gene involved in infantile spasms and mental retardation. J Biol Chem 2006; 281: 32048-32056
4. Mencarelli MA, Spanhol-Rosseto A, Artuso R, et al. Novel FOXG1 mutations associated with the congenital variant of Rett syndrome. J Med Genet 2010; 47: 49-53
5. Le Guen T, Bahi-Buisson N, Nectoux J, et al. A FOXG1 mutation in a boy with congenital variant of Rett syndrome. Neurogenetics 2011; 12: 1-8
6. Tian C, Gong Y, Yang Y, et al. Foxg1 has an essential role in postnatal development of the dentate gyrus. J Neurosci 2012; 32: 2931-2949
7. Eagleson KL, Schlueter McFadyen-Ketchum LJ, Ahrens ET, et al. Disruption of Foxg1 expression by knock-in of cre recombinase: effects on the development of the mouse telencephalon. Neuroscience 2007; 148: 385-399
8. Xuan S, Baptista CA, Balas G, Tao W, Soares VC, Lai E. Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron 1995; 14: 1141-1152
9. Shen L, Nam HS, Song P, Moore H, Anderson SA. FoxG1 haploinsufficiency results in impaired neurogenesis in the postnatal hippocampus and contextual memory deficits. Hippocampus 2006; 16: 875-890
10. Esmailpour T, Huang TS. TBX3 promotes human embryonic stem cell proliferation and neuroepithelial differentiation in a differentiation stage-dependent manner. Stem Cells 2012; 30: 2152-2163
11. Shibata M, Kurokawa D, Nakao H, Ohmura T, Aizawa S. MicroRNA-9 modulates Cajal-Retzius cell differentiation by suppressing Foxg1 expression in mouse medial pallium. J Neurosci 2008; 28: 10415-10421
12. Dastidar SG, Landrieu PM, D Mello SR. FoxG1 promotes the survival of postmitotic neurons. J Neurosci 2011; 31: 402-413
13. Martynoga B, Morrison H, Price DJ, Mason JO. Foxg1 is required for specification of ventral telencephalon and region-specific regulation of dorsal telencephalic precursor proliferation and apoptosis. Dev Biol 2005; 283: 113-127
14. Brunetti-Pierri N, Paciorkowski AR, Ciccone R, et al. Duplications of FOXG1 in 14q12 are associated with developmental epilepsy, mental retardation, and severe speech impairment. Eur J Hum Genet 2011; 19: 102-107
15. Pontrelli G, Cappelletti S, Claps D, et al. Epilepsy in patients with duplications of chromosome 14 harboring FOXG1. Pediatr Neurol 2014; 50: 530-535
16. Brancaccio M, Pivetta C, Granzotto M, Filippis C, Mallamaci A. Emx2 and Foxg1 inhibit gliogenesis and promote neuronogenesis. Stem Cells 2010; 28: 1206-1218
17. Raciti M, Granzotto M, Duc MD, et al. Reprogramming fibroblasts to neural-precursorlike cells by structured overexpression of pallial patterning genes. Mol Cell Neurosci 2013; 57: 42-53
18. Fasano CA, Phoenix TN, Kokovay E, et al. Bmi-1 cooperates with Foxg1 to maintain neural stem cell self-renewal in the forebrain. Genes Dev 2009; 23: 561-574
19. Yadirgi G, Leinster V, Acquati S, Bhagat H, Shakhova O, Marino S. Conditional activation of Bmi1 expression regulates self-renewal, apoptosis, and differentiation of neural stem/progenitor cells in vitro and in vivo. Stem Cells 2011; 29: 700-712
20. Regad T, Roth M, Bredenkamp N, Illing N, Papalopulu N. The neural progenitorspecifying activity of FoxG1 is antagonistically regulated by CKI and FGF. Nat Cell Biol 2007; 9: 531-540
21. Manuel MN, Martynoga B, Molinek MD, et al. The transcription factor Foxg1 regulates telencephalic progenitor proliferation cell autonomously, in part by controlling Pax6 expression levels. Neural Dev 2011; 6: 9
22. Pratt T, Quinn JC, Simpson TI, West JD, Mason JO, Price DJ. Disruption of early events in thalamocortical tract formation in mice lacking the transcription factors Pax6 or Foxg1. J Neurosci 2002; 22: 8523-8531
23. Pratt T, Vitalis T, Warren N, Edgar JM, Mason JO, Price DJ. A role for Pax6 in the normal development of dorsal thalamus and its cortical connections. Development 2000; 127: 5167-5178
24. Talamillo A, Quinn JC, Collinson JM, et al. Pax6 regulates regional development and neuronal migration in the cerebral cortex. Dev Biol 2003; 255: 151-163
25. Tyas DA, Pearson H, Rashbass P, Price DJ. Pax6 regulates cell adhesion during cortical development. Cereb Cortex 2003; 13: 612-619
26. Livide G, Patriarchi T, Amenduni M, et al. GluD1 is a common altered player in neuronal differentiation from both MECP2-mutated and CDKL5-mutated iPS cells. Eur J Hum Genet 2015; 23: 195-201
27. Kuroyanagi T, Yokoyama M, Hirano T. Postsynaptic glutamate receptor delta family contributes to presynaptic terminal differentiation and establishment of synaptic transmission. Proc Natl Acad Sci USA 2009; 106: 4912-4916
28. Yasumura M, Yoshida T, Lee SJ, Uemura T, Joo JY, Mishina M. Glutamate receptor delta1 induces preferentially inhibitory presynaptic differentiation of cortical neurons by interacting with neurexins through cerebellin precursor protein subtypes. J Neurochem 2012; 121: 705-716
29. Ryu K, Yokoyama M, Yamashita M, Hirano T. Induction of excitatory and inhibitory presynaptic differentiation by GluD1. Biochem Biophys Res Commun 2012; 417: 157-161
30. Konno K, Matsuda K, Nakamoto C, et al. Enriched expression of GluD1 in higher brain regions and its involvement in parallel fiber-interneuron synapse formation in the cerebellum. J Neurosci 2014; 34: 7412-7424
31. Cooper GM, Coe BP, Girirajan S, et al. A copy number variation morbidity map of developmental delay. Nat Genet 2011; 43: 838-846
32. Treutlein J, Muhleisen TW, Frank J, et al. Dissection of phenotype reveals possible association between schizophrenia and Glutamate Receptor Delta 1 (GRID1) gene promoter. Schizophr Res 2009; 111: 123-130
33. Pizzarelli R, Cherubini E. Alterations of GABAergic signaling in autism spectrum disorders. Neural Plast 2011; 2011: 297153
34. Tabuchi K, Blundell J, Etherton MR, et al. A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science 2007; 318: 71-76
35. Foldy C, Malenka RC, Sudhof TC. Autism-Associated neuroligin-3 mutations commonly disrupt tonic endocannabinoid signaling. Neuron 2013; 78: 498-509
36. Dracopoli N, Haines J, Korf B, et al. Current Protocols in Molecular Biology. Hoboken, NJ, USA: John Wiley & Son, 2000
37. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-872
38. Kim JE, O Sullivan ML, Sanchez CA, et al. Investigating synapse formation and function using human pluripotent stem cell-derived neurons. Proc Natl Acad Sci USA 2011; 108: 3005-3010
39. Yuan SH, Martin J, Elia J, et al. Cell-surface marker signatures for the isolation of neural stem cells, glia and neurons derived from human pluripotent stem cells. PLoS One 2011; 6: e17540
40. Hebert JM, McConnell SK. Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev Biol 2000; 222: 296-306
41. Siegenthaler JA, Tremper-Wells BA, Miller MW. Foxg1 haploinsufficiency reduces the population of cortical intermediate progenitor cells: effect of increased p21 expression. Cereb Cortex 2008; 18: 1865-1875
42. Zhubi A, Chen Y, Dong E, Cook EH, Guidotti A, Grayson DR. Increased binding of MeCP2 to the GAD1 and RELN promoters may be mediated by an enrichment of 5-hmC in autism spectrum disorder (ASD) cerebellum. Transl Psychiatry 2014; 4: e349
43. Dani VS, Chang Q, Maffei A, Turrigiano GG, Jaenisch R, Nelson SB. Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proc Natl Acad Sci USA 2005; 102: 12560-12565
44. Ricciardi S, Ungaro F, Hambrock M, et al. CDKL5 ensures excitatory synapse stability by reinforcing NGL-1-PSD95 interaction in the postsynaptic compartment and is impaired in patient iPSC-derived neurons. Nat Cell Biol 2012; 14: 911-923
45. Fernandez F, Morishita W, Zuniga E, et al. Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome. Nat Neurosci 2007; 10: 411-413
46. Na ES, Morris MJ, Nelson ED, Monteggia LM. GABAA receptor antagonism ameliorates behavioral and synaptic impairments associated with MeCP2 overexpression. Neuropsychopharmacology 2014; 39: 1946-1954
47. Zhang L, He J, Jugloff DG, Eubanks JH. The MeCP2-null mouse hippocampus displays altered basal inhibitory rhythms and is prone to hyperexcitability. Hippocampus 2008; 18: 294-309
48. Mariani J, Simonini MV, Palejev D, et al. Modeling human cortical development in vitro using induced pluripotent stem cells. Proc Natl Acad Sci USA 2012; 109: 12770-12775
49. Compagnucci C, Nizzardo M, Corti S, Zanni G, Bertini E. In vitro neurogenesis: development and functional implications of iPSC technology. Cell Mol Life Sci 2014; 71: 1623-1639
50. Kaufman MH. The Atlas of Mouse Development. London, San Diego: Academic Press, 1992
51. O Rahilly R. Early human development and the chief sources of information on staged human embryos. Eur J Obstet Gynecol Reprod Biol 1979; 9: 273-280
52. Abitz M, Nielsen RD, Jones EG, Laursen H, Graem N, Pakkenberg B. Excess of neurons in the human newborn mediodorsal thalamus compared with that of the adult. Cereb Cortex 2007; 17: 2573-2578
53. Chechik G, Meilijson I, Ruppin E. Synaptic pruning in development: a computational account. Neural Comput 1998; 10: 1759-1777
54. Chao HT, Chen H, Samaco RC, et al. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 2010; 468: 263-269
55. Akbarian S, Kim JJ, Potkin SG, et al. Gene-expression for glutamic-Acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch Gen Psychiatry 1995; 52: 258-266
56. Fatemi SH, Halt AR, Stary JM, Kanodia R, Schulz SC, Realmuto GR. Glutamic acid decarboxylase 65 and 67 kDa proteins are reduced in autistic parietal and cerebellar cortices. Biol Psychiatry 2002; 52: 805-810
57. El-Khoury R, Panayotis N, Matagne V, Ghata A, Villard L, Roux JC. GABA and glutamate pathways are spatially and developmentally affected in the brain of Mecp2-deficient mice. PLoS One 2014; 9: e92169
58. Yadav R, Gupta SC, Hillman BG, Bhatt JM, Stairs DJ, Dravid SM. Deletion of glutamate delta-1 receptor in mouse leads to aberrant emotional and social behaviors. PLoS One 2012; 7: e32969