Lhx6 directly regulates Arx and CXCR7 to determine cortical interneuron fate and laminar position

Neuron

Volumn 82, Issue 2, 2014, Pages 350-364

  Vogt, Daniel ^a   Hunt, Robert F ^b   Mandal, Shyamali ^a,c   Sandberg, Magnus ^a   Silberberg, Shanni N ^a   Nagasawa, Takashi ^d   Yang, Zhengang ^e   Baraban, Scott C ^b   Rubenstein, John L R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF ILLINOIS   (United States)

^d KYOTO UNIVERSITY   (Japan)

^e FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIALS; AGE FACTORS; ANIMALS; CELL MOVEMENT; CEREBRAL CORTEX; CHEMOKINE CXCL1; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HOMEODOMAIN PROTEINS; HUMANS; INTERNEURONS; LIM-HOMEODOMAIN PROTEINS; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; RECEPTORS, CXCR; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 84898678765     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.02.030     Document Type: Article

References (65)

1. Alcántara S., Ruiz M., D'Arcangelo G., Ezan F., de Lecea L., Curran T., Sotelo C., Soriano E. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J.Neurosci. 1998, 18:7779-7799.
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.R. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 1997, 278:474-476.
4. Ara T., Tokoyoda K., Sugiyama T., Egawa T., Kawabata K., Nagasawa T. Long-term hematopoietic stem cells require stromal cell-derived factor-1 for colonizing bone marrow during ontogeny. Immunity 2003, 19:257-267.
5. Arguello A., Yang X., Vogt D., Stanco A., Rubenstein J.L., Cheyette B.N. Dapper antagonist of catenin-1 cooperates with Dishevelled-1 during postsynaptic development in mouse forebrain GABAergic interneurons. PLoS ONE 2013, 8:e67679.
6. Armstrong C., Szabadics J., Tamás G., Soltesz I. Neurogliaform cells in the molecular layer of the dentate gyrus as feed-forward γ-aminobutyric acidergic modulators of entorhinal-hippocampal interplay. J.Comp. Neurol. 2011, 519:1476-1491.
7. 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.
8. 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.
9. Biressi S., Messina G., Collombat P., Tagliafico E., Monteverde S., Benedetti L., Cusella De Angelis M.G., Mansouri A., Ferrari S., Tajbakhsh S., et al. The homeobox gene Arx is a novel positive regulator of embryonic myogenesis. Cell Death Differ. 2008, 15:94-104.
10. Cai Y., Zhang Q., Wang C., Zhang Y., Ma T., Zhou X., Tian M., Rubenstein J.L., Yang Z. Nuclear receptor COUP-TFII-expressing neocortical interneurons are derived from the medial and lateral/caudal ganglionic eminence and define specific subsets of mature interneurons. J.Comp. Neurol. 2013, 521:479-497.
11. 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.
12. Chen Y.J., Vogt D., Wang Y., Visel A., Silberberg S.N., Nicholas C.R., Danjo T., Pollack J.L., Pennacchio L.A., Anderson S., et al. Use of "MGE enhancers" for labeling and selection of embryonic stem cell-derived medial ganglionic eminence (MGE) progenitors and neurons. PLoS ONE 2013, 8:e61956.
13. Choi G.B., Dong H.-W., Murphy A.J., Valenzuela D.M., Yancopoulos G.D., Swanson L.W., Anderson D.J. Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 2005, 46:647-660.
14. Chu Z., Galarreta M., Hestrin S. Synaptic interactions of late-spiking neocortical neurons in layer 1. J.Neurosci. 2003, 23:96-102.
15. 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.
16. Cobos I., Calcagnotto M.E., Vilaythong A.J., Thwin M.T., Noebels J.L., Baraban S.C., Rubenstein J.L.R. Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat. Neurosci. 2005, 8:1059-1068.
17. Cobos I., Borello U., Rubenstein J.L.R. Dlx transcription factors promote migration through repression of axon and dendrite growth. Neuron 2007, 54:873-888.
18. Colasante G., Collombat P., Raimondi V., Bonanomi D., Ferrai C., Maira M., Yoshikawa K., Mansouri A., Valtorta F., Rubenstein J.L.R., Broccoli V. Arx is a direct target of Dlx2 and thereby contributes to the tangential migration of GABAergic interneurons. J.Neurosci. 2008, 28:10674-10686.
19. 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.
20. Du T., Xu Q., Ocbina P.J., Anderson S.A. NKX2.1 specifies cortical interneuron fate by activating Lhx6. Development 2008, 135:1559-1567.
21. Elshatory Y., Gan L. The LIM-homeobox gene Islet-1 is required for the development of restricted forebrain cholinergic neurons. J.Neurosci. 2008, 28:3291-3297.
22. Flandin P., Kimura S., Rubenstein J.L. The progenitor zone of the ventral medial ganglionic eminence requires Nkx2-1 to generate most of the globus pallidus but few neocortical interneurons. J.Neurosci. 2010, 30:2812-2823.
23. Flandin P., Zhao Y., Vogt D., Jeong J., Long J., Potter G., Westphal H., Rubenstein J.L.R. Lhx6 and Lhx8 coordinately induce neuronal expression of Shh that controls the generation of interneuron progenitors. Neuron 2011, 70:939-950.
24. Fragkouli A., van Wijk N.V., Lopes R., Kessaris N., Pachnis V. LIM homeodomain transcription factor-dependent specification of bipotential MGE progenitors into cholinergic and GABAergic striatal interneurons. Development 2009, 136:3841-3851.
25. Gelman D., Griveau A., Dehorter N., Teissier A., Varela C., Pla R., Pierani A., Marín O. A wide diversity of cortical GABAergic interneurons derives from the embryonic preoptic area. J.Neurosci. 2011, 31:16570-16580.
26. Ghanem N., Jarinova O., Amores A., Long Q., Hatch G., Park B.K., Rubenstein J.L., Ekker M. Regulatory roles of conserved intergenic domains in vertebrate Dlx bigene clusters. Genome Res. 2003, 13:533-543.
27. Grigoriou M., Tucker A.S., Sharpe P.T., Pachnis V. Expression and regulation of Lhx6 and Lhx7, a novel subfamily of LIM homeodomain encoding genes, suggests a role in mammalian head development. Development 1998, 125:2063-2074.
28. 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.
29. 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.
30. Hunt R.F., Girskis K.M., Rubenstein J.L., Alvarez-Buylla A., Baraban S.C. GABA progenitors grafted into the adult epileptic brain control seizures and abnormal behavior. Nat. Neurosci. 2013, 16:692-697.
31. Jeong J., Li X., McEvilly R.J., Rosenfeld M.G., Lufkin T., Rubenstein J.L. Dlx genes pattern mammalian jaw primordium by regulating both lower jaw-specific and upper jaw-specific genetic programs. Development 2008, 135:2905-2916.
32. Kanatani S., Yozu M., Tabata H., Nakajima K. COUP-TFII is preferentially expressed in the caudal ganglionic eminence and is involved in the caudal migratory stream. J.Neurosci. 2008, 28:13582-13591.
33. Kimura N., Ueno M., Nakashima K., Taga T. A brain region-specific gene product Lhx6.1 interacts with Ldb1 through tandem LIM-domains. J.Biochem. 1999, 126:180-187.
34. Lee S., Hjerling-Leffler J., Zagha E., Fishell G., Rudy B. The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J.Neurosci. 2010, 30:16796-16808.
35. 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.
36. Long J.E., Cobos I., Potter G.B., Rubenstein J.L.R. Dlx1&2 and Mash1 transcription factors control MGE and CGE patterning and differentiation through parallel and overlapping pathways. Cereb. Cortex 2009, 19(Suppl 1):i96-i106.
37. Ma T., Zhang Q., Cai Y., You Y., Rubenstein J.L.R., Yang Z. A subpopulation of dorsal lateral/caudal ganglionic eminence-derived neocortical interneurons expresses the transcription factor Sp8. Cereb. Cortex 2012, 22:2120-2130.
38. 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.
39. Maroof A.M., Keros S., Tyson J.A., Ying S.W., Ganat Y.M., Merkle F.T., Liu B., Goulburn A., Stanley E.G., Elefanty A.G., et al. Directed differentiation and functional maturation of cortical interneurons from human embryonic stem cells. Cell Stem Cell 2013, 12:559-572.
40. McKinsey G.L., Lindtner S., Trzcinski B., Visel A., Pennacchio L.A., Huylebroeck D., Higashi Y., Rubenstein J.L. Dlx1&2-dependent expression of Zfhx1b (Sip1, Zeb2) regulates the fate switch between cortical and striatal interneurons. Neuron 2013, 77:83-98.
41. Miyoshi G., Fishell G. GABAergic interneuron lineages selectively sort into specific cortical layers during early postnatal development. Cereb. Cortex 2011, 21:845-852.
42. 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.
43. Nicholas C.R., Chen J., Tang Y., Southwell D.G., Chalmers N., Vogt D., Arnold C.M., Chen Y.J., Stanley E.G., Elefanty A.G., et al. Functional maturation of hPSC-derived forebrain interneurons requires an extended timeline and mimics human neural development. Cell Stem Cell 2013, 12:573-586.
44. 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.
45. Pueyo J.I., Couso J.P. Chip-mediated partnerships of the homeodomain proteins Bar and Aristaless with the LIM-HOM proteins Apterous andLim1 regulate distal leg development. Development 2004, 131:3107-3120.
46. Rubenstein J.L., Merzenich M.M. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2003, 2:255-267.
47. 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.
48. Sánchez-Alcañiz J.A., Haege S., Mueller W., Pla R., Mackay F., Schulz S., López-Bendito G., Stumm R., Marín O. Cxcr7 controls neuronal migration by regulating chemokine responsiveness. Neuron 2011, 69:77-90.
49. Schönemeier B., Kolodziej A., Schulz S., Jacobs S., Hoellt V., Stumm R. Regional and cellular localization of the CXCl12/SDF-1 chemokine receptor CXCR7 in the developing and adult rat brain. J.Comp. Neurol. 2008, 510:207-220.
50. Sierro F., Biben C., Martínez-Muñoz L., Mellado M., Ransohoff R.M., Li M., Woehl B., Leung H., Groom J., Batten M., et al. Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc. Natl. Acad. Sci. USA 2007, 104:14759-14764.
51. Stumm R.K., Zhou C., Ara T., Lazarini F., Dubois-Dalcq M., Nagasawa T., Höllt V., Schulz S. CXCR4 regulates interneuron migration in the developing neocortex. J.Neurosci. 2003, 23:5123-5130.
52. Sussel L., Marin O., Kimura S., Rubenstein J.L. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 1999, 126:3359-3370.
53. Tiveron M.C., Rossel M., Moepps B., Zhang Y.L., Seidenfaden R., Favor J., König N., Cremer H. Molecular interaction between projection neuron precursors and invading interneurons via stromal-derived factor 1 (CXCL12)/CXCR4 signaling in the cortical subventricular zone/intermediate zone. J.Neurosci. 2006, 26:13273-13278.
54. Tricoire L., Pelkey K.A., Daw M.I., Sousa V.H., Miyoshi G., Jeffries B., Cauli B., Fishell G., McBain C.J. Common origins of hippocampal Ivy and nitric oxide synthase expressing neurogliaform cells. J.Neurosci. 2010, 30:2165-2176.
55. Tricoire L., Pelkey K.A., Erkkila B.E., Jeffries B.W., Yuan X., McBain C.J. A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity. J.Neurosci. 2011, 31:10948-10970.
56. Vintersten K., Monetti C., Gertsenstein M., Zhang P., Laszlo L., Biechele S., Nagy A. Mouse in red: red fluorescent protein expression in mouse ES cells, embryos, and adult animals. Genesis 2004, 40:241-246.
57. Vokes S.A., Ji H., McCuine S., Tenzen T., Giles S., Zhong S., Longabaugh W.J.R., Davidson E.H., Wong W.H., McMahon A.P. Genomic characterization of Gli-activator targets in sonic hedgehog-mediated neural patterning. Development 2007, 134:1977-1989.
58. Wang Y., Li G., Stanco A., Long J.E., Crawford D., Potter G.B., Pleasure S.J., Behrens T., Rubenstein J.L.R. CXCR4 and CXCR7 have distinct functions in regulating interneuron migration. Neuron 2011, 69:61-76.
59. Wonders C.P., Anderson S.A. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 2006, 7:687-696.
60. Xu Q., Tam M., Anderson S.A. Fate mapping Nkx2.1-lineage cells in the mouse telencephalon. J.Comp. Neurol. 2008, 506:16-29.
61. Yizhar O., Fenno L.E., Prigge M., Schneider F., Davidson T.J., O'Shea D.J., Sohal V.S., Goshen I., Finkelstein J., Paz J.T., et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 2011, 477:171-178.
62. Zerucha T., Stuhmer T., Hatch G., Park B.K., Long Q., Yu G., Gambarotta A., Schultz J.R., Rubenstein J.L., Ekker M. A highly conserved enhancer in the Dlx5/Dlx6 intergenic region is the site of cross-regulatory interactions between Dlx genes in the embryonic forebrain. J.Neurosci. 2000, 20:709-721.
63. Zhao Y., Marín O., Hermesz E., Powell A., Flames N., Palkovits M., Rubenstein J.L., Westphal H. The LIM-homeobox gene Lhx8 is required for the development of many cholinergic neurons in the mouse forebrain. Proc. Natl. Acad. Sci. USA 2003, 100:9005-9010.
64. Zhao Y., Flandin P., Long J.E., Cuesta M.D., Westphal H., Rubenstein J.L.R. Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants. J.Comp. Neurol. 2008, 510:79-99.
65. Zhou F.M., Hablitz J.J. Rapid kinetics and inward rectification ofminiature EPSCs in layer I neurons of rat neocortex. J.Neurophysiol. 1997, 77:2416-2426.