The Parvalbumin/Somatostatin Ratio Is Increased in Pten Mutant Mice and by Human PTEN ASD Alleles

Cell Reports

Volumn 11, Issue 6, 2015, Pages 944-956

  Vogt, Daniel ^a   Cho, Kathleen K A ^a   Lee, Anthony T ^a   Sohal, Vikaas S ^a   Rubenstein, John L R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARVALBUMIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; SOMATOSTATIN; 4 AMINOBUTYRIC ACID RECEPTOR; CRE RECOMBINASE; INTEGRASE;

ALLELE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTISM; CELL PROLIFERATION; CELL SIZE; CONTROLLED STUDY; GABAERGIC SYSTEM; INTERNEURON; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PTEN GENE; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; WILD TYPE; ANIMAL; CELL COUNT; CELL DEATH; CELL SHAPE; ELECTROENCEPHALOGRAPHY; GAMMA RHYTHM; GENETICS; HUMAN; HUMAN RELATION; MEDIAN EMINENCE; METABOLISM; MUTATION; NEURAL STEM CELL;

MUS;

ALLELES; ANIMALS; AUTISM SPECTRUM DISORDER; CELL COUNT; CELL DEATH; CELL PROLIFERATION; CELL SHAPE; ELECTROENCEPHALOGRAPHY; GABAERGIC NEURONS; GAMMA RHYTHM; HUMANS; INTEGRASES; INTERNEURONS; INTERPERSONAL RELATIONS; MEDIAN EMINENCE; MICE; MUTATION; NEURAL STEM CELLS; PARVALBUMINS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; PYRAMIDAL CELLS; SIGNAL TRANSDUCTION; SOMATOSTATIN;

EID: 84929274006     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.04.019     Document Type: Article

References (57)

1. Allegra M., Genovesi S., Maggia M., Cenni M.C., Zunino G., Sgadò P., Caleo M., Bozzi Y. Altered GABAergic markers, increased binocularity and reduced plasticity in the visual cortex of Engrailed-2 knockout mice. Front. Cell. Neurosci. 2014, 8:163.
2. Alvarez-Dolado M., Calcagnotto M.E., Karkar K.M., Southwell D.G., Jones-Davis D.M., Estrada R.C., Rubenstein J.L.R., Alvarez-Buylla A., Baraban S.C. Cortical inhibition modified by embryonic neural precursors grafted into the postnatal brain. J.Neurosci. 2006, 26:7380-7389.
3. Anderson S.A., Eisenstat D.D., Shi L., Rubenstein J.L. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 1997, 278:474-476.
4. Arguello A., Yang X., Vogt D., Stanco A., Rubenstein J.L.R., Cheyette B.N.R. Dapper antagonist of catenin-1 cooperates with Dishevelled-1 during postsynaptic development in mouse forebrain GABAergic interneurons. PLoS ONE 2013, 8:e67679.
5. Bourgeron T. A synaptic trek to autism. Curr. Opin. Neurobiol. 2009, 19:231-234.
6. Butler M.G., Dasouki M.J., Zhou X.-P., Talebizadeh Z., Brown M., Takahashi T.N., Miles J.H., Wang C.H., Stratton R., Pilarski R., Eng C. Subset of individuals with autism spectrum disorders and extreme macrocephaly associated with germline PTEN tumour suppressor gene mutations. J.Med. Genet. 2005, 42:318-321.
7. Cardin J.A., Carlén M., Meletis K., Knoblich U., Zhang F., Deisseroth K., Tsai L.-H., Moore C.I. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 2009, 459:663-667.
8. Chao H.-T., Chen H., Samaco R.C., Xue M., Chahrour M., Yoo J., Neul J.L., Gong S., Lu H.-C., Heintz N., et al. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 2010, 468:263-269.
9. Close J., Xu H., De Marco García N., Batista-Brito R., Rossignol E., Rudy B., Fishell G. Satb1 is an activity-modulated transcription factor required for the terminal differentiation and connectivity of medial ganglionic eminence-derived cortical interneurons. J.Neurosci. 2012, 32:17690-17705.
10. Cobos I., Calcagnotto M.E., Vilaythong A.J., Thwin M.T., Noebels J.L., Baraban S.C., Rubenstein J.L. Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat. Neurosci. 2005, 8:1059-1068.
11. Costa R.M., Federov N.B., Kogan J.H., Murphy G.G., Stern J., Ohno M., Kucherlapati R., Jacks T., Silva A.J. Mechanism for the learning deficits in a mouse model of neurofibromatosis type 1. Nature 2002, 415:526-530.
12. Cui Y., Costa R.M., Murphy G.G., Elgersma Y., Zhu Y., Gutmann D.H., Parada L.F., Mody I., Silva A.J. Neurofibromin regulation of ERK signaling modulates GABA release and learning. Cell 2008, 135:549-560.
13. Denaxa M., Kalaitzidou M., Garefalaki A., Achimastou A., Lasrado R., Maes T., Pachnis V. Maturation-promoting activity of SATB1 in MGE-derived cortical interneurons. Cell Rep. 2012, 2:1351-1362.
14. Du J., Zhang L., Weiser M., Rudy B., McBain C.J. Developmental expression and functional characterization of the potassium-channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus. J.Neurosci. 1996, 16:506-518.
15. Durand S., Patrizi A., Quast K.B., Hachigian L., Pavlyuk R., Saxena A., Carninci P., Hensch T.K., Fagiolini M. NMDA receptor regulation prevents regression of visual cortical function in the absence of Mecp2. Neuron 2012, 76:1078-1090.
16. Fraser M.M., Bayazitov I.T., Zakharenko S.S., Baker S.J. Phosphatase and tensin homolog, deleted on chromosome 10 deficiency in brain causes defects in synaptic structure, transmission and plasticity, and myelination abnormalities. Neuroscience 2008, 151:476-488.
17. Gandal M.J., Edgar J.C., Ehrlichman R.S., Mehta M., Roberts T.P.L., Siegel S.J. Validating γ oscillations and delayed auditory responses as translational biomarkers of autism. Biol. Psychiatry 2010, 68:1100-1106.
18. Gogolla N., Takesian A.E., Feng G., Fagiolini M., Hensch T.K. Sensory integration in mouse insular cortex reflects GABA circuit maturation. Neuron 2014, 83:894-905.
19. Hamilton S.P., Woo J.M., Carlson E.J., Ghanem N., Ekker M., Rubenstein J.L. Analysis of four DLX homeobox genes in autistic probands. BMC Genet. 2005, 6:52.
20. Han S., Tai C., Westenbroek R.E., Yu F.H., Cheah C.S., Potter G.B., Rubenstein J.L., Scheuer T., de la Iglesia H.O., Catterall W.A. Autistic-like behaviour in Scn1a+/- mice and rescue by enhanced GABA-mediated neurotransmission. Nature 2012, 489:385-390.
21. Huang Z.J., Di Cristo G., Ango F. Development of GABA innervation in the cerebral and cerebellar cortices. Nat. Rev. Neurosci. 2007, 8:673-686.
22. Karayannis T., Au E., Patel J.C., Kruglikov I., Markx S., Delorme R., Héron D., Salomon D., Glessner J., Restituito S., et al. Cntnap4 differentially contributes to GABAergic and dopaminergic synaptic transmission. Nature 2014, 511:236-240.
23. Kölsch V., Charest P.G., Firtel R.A. The regulation of cell motility and chemotaxis by phospholipid signaling. J.Cell Sci. 2008, 121:551-559.
24. Kwon C.H., Luikart B.W., Powell C.M., Zhou J., Matheny S.A., Zhang W., Li Y., Baker S.J., Parada L.F. Pten regulates neuronal arborization and social interaction in mice. Neuron 2006, 50:377-388.
25. Ljungberg M.C., Sunnen C.N., Lugo J.N., Anderson A.E., D'Arcangelo G. Rapamycin suppresses seizures and neuronal hypertrophy in a mouse model of cortical dysplasia. Dis. Model. Mech. 2009, 2:389-398.
26. Luikart B.W., Schnell E., Washburn E.K., Bensen A.L., Tovar K.R., Westbrook G.L. Pten knockdown invivo increases excitatory drive onto dentate granule cells. J.Neurosci. 2011, 31:4345-4354.
27. Madisen L., Zwingman T.A., Sunkin S.M., Oh S.W., Zariwala H.A., Gu H., Ng L.L., Palmiter R.D., Hawrylycz M.J., Jones A.R., et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 2010, 13:133-140.
28. Marui T., Hashimoto O., Nanba E., Kato C., Tochigi M., Umekage T., Ishijima M., Kohda K., Kato N., Sasaki T. Association between the neurofibromatosis-1 (NF1) locus and autism in the Japanese population. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 2004, 131B:43-47.
29. Mbarek O., Marouillat S., Martineau J., Barthélémy C., Müh J.P., Andres C. Association study of the NF1 gene and autistic disorder. Am. J. Med. Genet. 1999, 88:729-732.
30. Miyoshi G., Hjerling-Leffler J., Karayannis T., Sousa V.H., Butt S.J.B., Battiste J., Johnson J.E., Machold R.P., Fishell G. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J.Neurosci. 2010, 30:1582-1594.
31. Murdoch J.D., State M.W. Recent developments in the genetics of autism spectrum disorders. Curr. Opin. Genet. Dev. 2013, 23:310-315.
32. Neves G., Shah M.M., Liodis P., Achimastou A., Denaxa M., Roalfe G., Sesay A., Walker M.C., Pachnis V. The LIM homeodomain protein Lhx6 regulates maturation of interneurons and network excitability in the mammalian cortex. Cereb. Cortex 2013, 23:1811-1823.
33. O'Roak B.J., Vives L., Fu W., Egertson J.D., Stanaway I.B., Phelps I.G., Carvill G., Kumar A., Lee C., Ankenman K., et al. Multiplex targeted sequencing identifies recurrently mutated genes in autism spectrum disorders. Science 2012, 338:1619-1622.
34. Orekhova E.V., Stroganova T.A., Nygren G., Tsetlin M.M., Posikera I.N., Gillberg C., Elam M. Excess of high frequency electroencephalogram oscillations in boys with autism. Biol. Psychiatry 2007, 62:1022-1029.
35. Orrico A., Galli L., Buoni S., Orsi A., Vonella G., Sorrentino V. Novel PTEN mutations in neurodevelopmental disorders and macrocephaly. Clin. Genet. 2009, 75:195-198.
36. Peñagarikano O., Abrahams B.S., Herman E.I., Winden K.D., Gdalyahu A., Dong H., Sonnenblick L.I., Gruver R., Almajano J., Bragin A., et al. Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities, and core autism-related deficits. Cell 2011, 147:235-246.
37. Pesold C., Liu W.S., Guidotti A., Costa E., Caruncho H.J. Cortical bitufted, horizontal, and Martinotti cells preferentially express and secrete reelin into perineuronal nets, nonsynaptically modulating gene expression. Proc. Natl. Acad. Sci. USA 1999, 96:3217-3222.
38. Potter G.B., Petryniak M.A., Shevchenko E., McKinsey G.L., Ekker M., Rubenstein J.L.R. Generation of Cre-transgenic mice using Dlx1/Dlx2 enhancers and their characterization in GABAergic interneurons. Mol. Cell. Neurosci. 2009, 40:167-186.
39. Rodríguez-Escudero I., Oliver M.D., Andrés-Pons A., Molina M., Cid V.J., Pulido R. A comprehensive functional analysis of PTEN mutations: implications in tumor- and autism-related syndromes. Hum. Mol. Genet. 2011, 20:4132-4142.
40. Rubenstein J.L.R., Merzenich M.M. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2003, 2:255-267.
41. Selby L., Zhang C., Sun Q.Q. Major defects in neocortical GABAergic inhibitory circuits in mice lacking the fragile X mental retardation protein. Neurosci. Lett. 2007, 412:227-232.
42. Silbereis J.C., Nobuta H., Tsai H.H., Heine V.M., McKinsey G.L., Meijer D.H., Howard M.A., Petryniak M.A., Potter G.B., Alberta J.A., et al. Olig1 function is required to repress dlx1/2 and interneuron production in Mammalian brain. Neuron 2014, 81:574-587.
43. Sohal V.S., Huguenard J.R. Inhibitory coupling specifically generates emergent gamma oscillations in diverse cell types. Proc. Natl. Acad. Sci. USA 2005, 102:18638-18643.
44. Sohal V.S., Zhang F., Yizhar O., Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 2009, 459:698-702.
45. Stanco A., Pla R., Vogt D., Chen Y., Mandal S., Walker J., Hunt R.F., Lindtner S., Erdman C.A., Pieper A.A., et al. NPAS1 represses the generation of specific subtypes of cortical interneurons. Neuron 2014, 84:940-953.
46. Stiles B.L. Phosphatase and tensin homologue deleted on chromosome 10: extending its PTENtacles. Int. J. Biochem. Cell Biol. 2009, 41:757-761.
47. Suzuki A., Yamaguchi M.T., Ohteki T., Sasaki T., Kaisho T., Kimura Y., Yoshida R., Wakeham A., Higuchi T., Fukumoto M., et al. T cell-specific loss of Pten leads to defects in central and peripheral tolerance. Immunity 2001, 14:523-534.
48. Taniguchi H., He M., Wu P., Kim S., Paik R., Sugino K., Kvitsiani D., Fu Y., Lu J., Lin Y., et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 2011, 71:995-1013.
49. Tebbenkamp A.T.N., Willsey A.J., State M.W., Sestan N. The developmental transcriptome of the human brain: implications for neurodevelopmental disorders. Curr. Opin. Neurol. 2014, 27:149-156.
50. Vogt D., Hunt R.F., Mandal S., Sandberg M., Silberberg S.N., Nagasawa T., Yang Z., Baraban S.C., Rubenstein J.L.R. Lhx6 directly regulates Arx and CXCR7 to determine cortical interneuron fate and laminar position. Neuron 2014, 82:350-364.
51. Vogt D., Wu P.-R., Sorrells S.F., Arnold C., Alvarez-Buylla A., Rubenstein J.L.R. Viral-mediated labeling and transplantation of medial ganglionic eminence (MGE) cells for invivo studies. J.Vis. Exp. 2015, Published online April 23, 2015. 10.3791/52740.
52. Williams M.R., DeSpenza T., Li M., Gulledge A.T., Luikart B.W. Hyperactivity of newborn Pten knock-out neurons results from increased excitatory synaptic drive. J.Neurosci. 2015, 35:943-959.
53. Wilson T.W., Rojas D.C., Reite M.L., Teale P.D., Rogers S.J. Children and adolescents with autism exhibit reduced MEG steady-state gamma responses. Biol. Psychiatry 2007, 62:192-197.
54. Wiznitzer M. Autism and tuberous sclerosis. J.Child Neurol. 2004, 19:675-679.
55. Wonders C.P., Anderson S.A. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 2006, 7:687-696.
56. Xu Q., Tam M., Anderson S.A. Fate mapping Nkx2.1-lineage cells in the mouse telencephalon. J.Comp. Neurol. 2008, 506:16-29.
57. Zhou J., Blundell J., Ogawa S., Kwon C.-H., Zhang W., Sinton C., Powell C.M., Parada L.F. Pharmacological inhibition of mTORC1 suppresses anatomical, cellular, and behavioral abnormalities in neural-specific Pten knock-out mice. J.Neurosci. 2009, 29:1773-1783.