Maturation-Promoting Activity of SATB1 in MGE-Derived Cortical Interneurons

Cell Reports

Volumn 2, Issue 5, 2012, Pages 1351-1362

  Denaxa, Myrto ^a   Kalaitzidou, Melanie ^a   Garefalaki, Anna ^a,c   Achimastou, Angeliki ^a   Lasrado, Reena ^a   Maes, Tamara ^b   Pachnis, Vassilis ^a,c  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b ORYZON GENOMICS   (Spain)

^c INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

REGULATOR PROTEIN; SOMATOSTATIN; SPECIAL AT RICH DNA BINDING PROTEIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL ACTIVITY; CELL FUNCTION; CELL MATURATION; CELL MIGRATION; CELL NUCLEUS; CONTROLLED STUDY; EMBRYO; EPIGENETICS; GENE; INTERNEURON; LHX6 GENE; MEDIAN EMINENCE; MOLECULAR BIOLOGY; MOLECULAR GENETICS; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBRAL CORTEX; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; GENE EXPRESSION PROFILING; GLUTAMATE DECARBOXYLASE; INTERNEURONS; LIM-HOMEODOMAIN PROTEINS; MATRIX ATTACHMENT REGION BINDING PROTEINS; MICE; NERVE TISSUE PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SOMATOSTATIN; TRANSCRIPTION FACTORS;

MAMMALIA; MUS;

EID: 84870474577     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2012.10.003     Document Type: Article

References (50)

1. Alvarez J.D., Yasui D.H., Niida H., Joh T., Loh D.Y., Kohwi-Shigematsu T. The MAR-binding protein SATB1 orchestrates temporal and spatial expression of multiple genes during T-cell development. Genes Dev. 2000, 14:521-535.
2. Azim E., Jabaudon D., Fame R.M., Macklis J.D. SOX6 controls dorsal progenitor identity and interneuron diversity during neocortical development. Nat. Neurosci. 2009, 12:1238-1247.
3. Balamotis M.A., Tamberg N., Woo Y.J., Li J., Davy B., Kohwi-Shigematsu T., Kohwi Y. Satb1 ablation alters temporal expression of immediate early genes and reduces dendritic spine density during postnatal brain development. Mol. Cell. Biol. 2012, 32:333-347.
4. Batista-Brito R., Fishell G. The developmental integration of cortical interneurons into a functional network. Curr. Top. Dev. Biol. 2009, 87:81-118.
5. Batista-Brito R., Rossignol E., Hjerling-Leffler J., Denaxa M., Wegner M., Lefebvre V., Pachnis V., Fishell G. The cell-intrinsic requirement of Sox6 for cortical interneuron development. Neuron 2009, 63:466-481.
6. Bellion A., Baudoin J.P., Alvarez C., Bornens M., Métin C. Nucleokinesis in tangentially migrating neurons comprises two alternating phases: forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear. J. Neurosci. 2005, 25:5691-5699.
7. Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat. Rev. Neurosci. 2002, 3:728-739.
8. Ben-Ari Y., Spitzer N.C. Phenotypic checkpoints regulate neuronal development. Trends Neurosci. 2010, 33:485-492.
9. Ben-Ari Y., Gaiarsa J.L., Tyzio R., Khazipov R. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 2007, 87:1215-1284.
10. Bortone D., Polleux F. KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. Neuron 2009, 62:53-71.
11. Burbach J.P. Regulation of gene promoters of hypothalamic peptides. Front. Neuroendocrinol. 2002, 23:342-369.
12. Butt S.J., Fuccillo M., Nery S., Noctor S., Kriegstein A., Corbin J.G., Fishell G. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 2005, 48:591-604.
13. Cai S., Han H.J., Kohwi-Shigematsu T. Tissue-specific nuclear architecture and gene expression regulated by SATB1. Nat. Genet. 2003, 34:42-51.
14. Cai S., Lee C.C., Kohwi-Shigematsu T. SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes. Nat. Genet. 2006, 38:1278-1288.
15. Chen L., Liao G., Waclaw R.R., Burns K.A., Linquist D., Campbell K., Zheng Y., Kuan C.Y. Rac1 controls the formation of midline commissures and the competency of tangential migration in ventral telencephalic neurons. J. Neurosci. 2007, 27:3884-3893.
16. Chow A., Erisir A., Farb C., Nadal M.S., Ozaita A., Lau D., Welker E., Rudy B. K(+) channel expression distinguishes subpopulations of parvalbumin- and somatostatin-containing neocortical interneurons. J. Neurosci. 1999, 19:9332-9345.
17. Corlew R., Bosma M.M., Moody W.J. Spontaneous, synchronous electrical activity in neonatal mouse cortical neurones. J. Physiol. 2004, 560:377-390.
18. Cossart R. The maturation of cortical interneuron diversity: how multiple developmental journeys shape the emergence of proper network function. Curr. Opin. Neurobiol. 2011, 21:160-168.
19. del Río J.A., de Lecea L., Ferrer I., Soriano E. The development of parvalbumin-immunoreactivity in the neocortex of the mouse. Brain Res. Dev. Brain Res. 1994, 81:247-259.
20. Fazzari P., Paternain A.V., Valiente M., Pla R., Luján R., Lloyd K., Lerma J., Marín O., Rico B. Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 2010, 464:1376-1380.
21. Flames N., Long J.E., Garratt A.N., Fischer T.M., Gassmann M., Birchmeier C., Lai C., Rubenstein J.L., Marín O. Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 2004, 44:251-261.
22. Fogarty M., Grist M., Gelman D., Marín O., Pachnis V., Kessaris N. Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J. Neurosci. 2007, 27:10935-10946.
23. Han H.J., Russo J., Kohwi Y., Kohwi-Shigematsu T. SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 2008, 452:187-193.
24. Huang Y., Zhang L., Song N.N., Hu Z.L., Chen J.Y., Ding Y.Q. Distribution of Satb1 in the central nervous system of adult mice. Neurosci. Res. 2011, 71:12-21.
25. Inada H., Watanabe M., Uchida T., Ishibashi H., Wake H., Nemoto T., Yanagawa Y., Fukuda A., Nabekura J. GABA regulates the multidirectional tangential migration of GABAergic interneurons in living neonatal mice. PLoS ONE 2011, 6:e27048.
26. Jiang M., Swann J.W. A role for L-type calcium channels in the maturation of parvalbumin-containing hippocampal interneurons. Neuroscience 2005, 135:839-850.
27. Kawaguchi Y., Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 1997, 7:476-486.
28. Kessaris N., Fogarty M., Iannarelli P., Grist M., Wegner M., Richardson W.D. Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat. Neurosci. 2006, 9:173-179.
29. Kubota Y., Shigematsu N., Karube F., Sekigawa A., Kato S., Yamaguchi N., Hirai Y., Morishima M., Kawaguchi Y. Selective coexpression of multiple chemical markers defines discrete populations of neocortical GABAergic neurons. Cereb. Cortex 2011, 21:1803-1817.
30. Kwan K.Y., Lam M.M., Johnson M.B., Dube U., Shim S., RaŠin M.R., Sousa A.M., Fertuzinhos S., Chen J.G., Arellano J.I., et al. Species-dependent posttranscriptional regulation of NOS1 by FMRP in the developing cerebral cortex. Cell 2012, 149:899-911.
31. Liodis P., Denaxa M., Grigoriou M., Akufo-Addo C., Yanagawa Y., Pachnis V. Lhx6 activity is required for the normal migration and specification of cortical interneuron subtypes. J. Neurosci. 2007, 27:3078-3089.
32. Markram H., Toledo-Rodriguez M., Wang Y., Gupta A., Silberberg G., Wu C., Monyer H. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 2004, 5:793-807.
33. Miyoshi G., Butt S.J., Takebayashi H., Fishell G. Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors. J. Neurosci. 2007, 27:7786-7798.
34. Miyoshi G., Hjerling-Leffler J., Karayannis T., Sousa V.H., Butt S.J., 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.
35. Moody W.J., Bosma M.M. Ion channel development, spontaneous activity, and activity-dependent development in nerve and muscle cells. Physiol. Rev. 2005, 85:883-941.
36. Neddens J., Buonanno A. Selective populations of hippocampal interneurons express ErbB4 and their number and distribution is altered in ErbB4 knockout mice. Hippocampus 2010, 20:724-744.
37. 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. 2012, Published online June 17, 2012.
38. Perrenoud Q., Geoffroy H., Gauthier B., Rancillac A., Alfonsi F., Kessaris N., Rossier J., Vitalis T., Gallopin T. Characterization of type I and type II nNOS-expressing interneurons in the barrel cortex of mouse. Frontiers Neural Circuits 2012, 6:36.
39. Rudy B., Fishell G., Lee S., Hjerling-Leffler J. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 2011, 71:45-61.
40. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001, 1:4.
41. Tanaka D., Nakaya Y., Yanagawa Y., Obata K., Murakami F. Multimodal tangential migration of neocortical GABAergic neurons independent of GPI-anchored proteins. Development 2003, 130:5803-5813.
42. 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.
43. Todd P.K., Mack K.J., Malter J.S. The fragile X mental retardation protein is required for type-I metabotropic glutamate receptor-dependent translation of PSD-95. Proc. Natl. Acad. Sci. USA 2003, 100:14374-14378.
44. Tomioka R., Okamoto K., Furuta T., Fujiyama F., Iwasato T., Yanagawa Y., Obata K., Kaneko T., Tamamaki N. Demonstration of long-range GABAergic connections distributed throughout the mouse neocortex. Eur. J. Neurosci. 2005, 21:1587-1600.
45. Tuy F.P., Saillour Y., Kappeler C., Chelly J., Francis F. Alternative transcripts of Dclk1 and Dclk2 and their expression in doublecortin knockout mice. Dev. Neurosci. 2008, 30:171-186.
46. Welagen J., Anderson S. Origins of neocortical interneurons in mice. Dev. Neurobiol. 2011, 71:10-17.
47. Wonders C.P., Anderson S.A. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 2006, 7:687-696.
48. Xu Q., Guo L., Moore H., Waclaw R.R., Campbell K., Anderson S.A. Sonic hedgehog signaling confers ventral telencephalic progenitors with distinct cortical interneuron fates. Neuron 2010, 65:328-340.
49. Yamada J., Okabe A., Toyoda H., Kilb W., Luhmann H.J., Fukuda A. Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J. Physiol. 2004, 557:829-841.
50. Zhao Y., Flandin P., Long J.E., Cuesta M.D., Westphal H., Rubenstein J.L. Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants. J. Comp. Neurol. 2008, 510:79-99.