The germinal zones of the basal ganglia but not the septum generate GABAergic interneurons for the cortex

Journal of Neuroscience

Volumn 30, Issue 36, 2010, Pages 12050-12062

  Rubin, Anna N ^a   Alfonsi, Fabienne ^a   Humphreys, Michael P ^a   Choi, Christina K P ^a   Rocha, Susana F ^a,b   Kessaris, Nicoletta ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BASAL GANGLION; BRAIN CORTEX; CELL MIGRATION; CELL POPULATION; CONTROLLED STUDY; GABAERGIC SYSTEM; GANGLION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERNEURON; MOUSE; NEOCORTEX; NEUROCHEMISTRY; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; SUBVENTRICULAR ZONE; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CELL MOTION; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEWBORN; PHYSIOLOGY; SEPTUM PELLUCIDUM; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; BASAL GANGLIA; CELL MOVEMENT; CEREBRAL CORTEX; EMBRYO, MAMMALIAN; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; INTERNEURONS; LUMINESCENT PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PROTEINS; SEPTUM OF BRAIN; TRANSCRIPTION FACTORS; LIM-HOMEODOMAIN PROTEINS; RNA, UNTRANSLATED;

4 AMINOBUTYRIC ACID; DISTAL-LESS HOMEOBOX PROTEINS; GREEN FLUORESCENT PROTEIN; GT(ROSA)26SOR NON-CODING RNA, MOUSE; HOMEODOMAIN PROTEIN; LHX6 PROTEIN, MOUSE; LIM HOMEODOMAIN PROTEIN; NERVE PROTEIN; NUCLEAR PROTEIN; PHOTOPROTEIN; PROTEIN; THYROID NUCLEAR FACTOR 1; TRANSCRIPTION FACTOR; UNTRANSLATED RNA; ZIC4 PROTEIN, MOUSE;

EID: 77956605472     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6178-09.2010     Document Type: Article

References (62)

1. Anderson S, Mione M, Yun K, Rubenstein JL (1999) Differential origins of neocortical projection and local circuit neurons: role of Dlx genes in neocortical interneuronogenesis. Cereb Cortex 9:646-654.
2. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL (1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476.
3. Ang ES Jr, Haydar TF, Gluncic V, Rakic P (2003) Four-dimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex. J Neurosci 23:5805-5815.
4. Aruga J (2004) The role of Zic genes in neural development. Mol Cell Neurosci 26:205-221. (Pubitemid 38781079)
5. Batista-Brito R, Fishell G (2009) The developmental integration of cortical interneurons into a functional network. Curr Top Dev Biol 87:81-118.
6. Bielle F, Griveau A, Narboux-Nême N, Vigneau S, Sigrist M, Arber S, Wassef M, Pierani A (2005) Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat Neurosci 8:1002-1012.
7. Bulfone A, Puelles L, Porteus MH, Frohman MA, Martin GR, Rubenstein JL (1993) Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J Neurosci 13:3155-3172.
8. Butt SJ, Fuccillo M, Nery S, Noctor S, Kriegstein A, Corbin JG, Fishell G (2005) The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48:591-604.
9. Cobos I, Calcagnotto ME, Vilaythong AJ, Thwin MT, Noebels JL, Baraban SC, Rubenstein JL (2005) Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat Neurosci 8:1059-1068.
10. Cobos I, Long JE, Thwin MT, Rubenstein JL (2006) Cellular patterns of transcription factor expression in developing cortical interneurons. Cereb Cortex 16 [Suppl 1]:i82-i88.
11. Cobos I, Borello U, Rubenstein JL (2007) Dlx transcription factors promote migration through repression of axon and dendrite growth. Neuron 54:873-888. (Pubitemid 46907500)
12. Du T, Xu Q, Ocbina PJ, Anderson SA (2008) NKX2.1 specifies cortical interneuron fate by activating Lhx6. Development 135:1559-1567.
13. Eisenstat DD, Liu JK, Mione M, Zhong W, Yu G, Anderson SA, Ghattas I, Puelles L, Rubenstein JL (1999) DLX-1, DLX-2, and DLX-5 expression define distinct stages of basal forebrain differentiation. J Comp Neurol 414:217-237.
14. Flames N, Long JE, Garratt AN, Fischer TM, Gassmann M, Birchmeier C, Lai C, Rubenstein JL, Marín O (2004) Short-and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44:251-261.
15. Flames N, Pla R, Gelman DM, Rubenstein JL, Puelles L, Marín O (2007) Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J Neurosci 27:9682-9695.
16. Fogarty M, Grist M, Gelman D, Marín O, Pachnis V, Kessaris N (2007) Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J Neurosci 27:10935-10946. (Pubitemid 47574155)
17. Gaston-Massuet C, Henderson DJ, Greene ND, Copp AJ (2005) Zic4, a zinc-finger transcription factor, is expressed in the developing mouse nervous system. Dev Dyn 233:1110-1115.
18. Gelman DM, Martini FJ, Nó brega-Pereira S, Pierani A, Kessaris N, Marín O (2009) The embryonic preoptic area is a novel source of cortical GABAergic interneurons. J Neurosci 29:9380-9389.
19. Inoue T, Ota M, Ogawa M, Mikoshiba K, Aruga J (2007) Zic1 and Zic3 regulate medial forebrain development through expansion of neuronal progenitors. J Neurosci 27:5461-5473.
20. Inoue T, Ogawa M, Mikoshiba K, Aruga J (2008) Zic deficiency in the cortical marginal zone and meninges results in cortical lamination defects resembling those in type II lissencephaly. J Neurosci 28:4712-4725.
21. Kanatani S, Yozu M, Tabata H, Nakajima K (2008) COUP-TFII is preferentially expressed in the caudal ganglionic eminence and is involved in the caudal migratory stream. J Neurosci 28:13582-13591.
22. Kessaris N, Fogarty M, Iannarelli P, Grist M, Wegner M, Richardson WD (2006) Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat Neurosci 9:173-179.
23. Lavdas AA, Grigoriou M, Pachnis V, Parnavelas JG (1999) The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci 19:7881-7888. (Pubitemid 30225786)
24. Le TN, Du G, Fonseca M, Zhou QP, Wigle JT, Eisenstat DD (2007) DLX homeobox genes promote cortical interneuron migration from the basal forebrain by direct repression of the semaphorin receptor neuropilin-2. J Biol Chem 282:19071-19081.
25. Lee EC, Yu D, Martinez de Velasco J, Tessarollo L, Swing DA, Court DL, Jenkins NA, Copeland NG (2001) A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73:56-65.
26. Li G, Adesnik H, Li J, Long J, Nicoll RA, Rubenstein JL, Pleasure SJ (2008) Regional distribution of cortical interneurons and development of inhibitory tone are regulated by Cxcl12/Cxcr4 signaling. J Neurosci 28:1085-1098.
27. Liu X, Novosedlik N, Wang A, Hudson ML, Cohen IL, Chudley AE, Forster-Gibson CJ, Lewis SM, Holden JJ (2009) The DLX1and DLX2 genes and susceptibility to autism spectrum disorders. Eur J Hum Genet 17:228-235.
28. López-Bendito G, Sánchez-Alcañiz JA, Pla R, Borrell V, Picó E, Valdeolmillos M, Marín O (2008) Chemokine signaling controls intracortical migration and final distribution of GABAergic interneurons. J Neurosci 28:1613-1624.
29. Mao X, Fujiwara Y, Chapdelaine A, Yang H, Orkin SH (2001) Activation of EGFP expression by Cre-mediated excision in a new ROSA26 reporter mouse strain. Blood 97:324-326.
30. Maurus D, Harris WA (2009) Zic-associated holoprosencephaly: zebrafish Zic1 controls midline formation and forebrain patterning by regulating Nodal, Hedgehog, and retinoic acid signaling. Genes Dev 23:1461-1473.
31. Miyoshi G, Butt SJ, Takebayashi H, Fishell G (2007) Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors. J Neurosci 27:7786-7798. (Pubitemid 47093809)
32. Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J, Johnson JE, Machold RP, Fishell G (2010) Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 30:1582-1594.
33. Nadarajah B, Alifragis P, Wong RO, Parnavelas JG (2002) Ventricle-directed migration in the developing cerebral cortex. Nat Neurosci 5:218-224. (Pubitemid 34171134)
34. Nagai T, Aruga J, Takada S, Günther T, Spörle R, Schughart K, Mikoshiba K (1997) The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation. Dev Biol 182:299-313.
35. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20:87-90.
36. Nery S, Fishell G, Corbin JG (2002) The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci 5:1279-1287.
37. Petryniak MA, Potter GB, Rowitch DH, Rubenstein JL (2007) Dlx1 and Dlx2 control neuronal versus oligodendroglial cell fate acquisition in the developing forebrain. Neuron 55:417-433.
38. Shimshek DR, Kim J, Hübner MR, Spergel DJ, Buchholz F, Casanova E, Stewart AF, Seeburg PH, Sprengel R (2002) Codon-improved Cre recombinase (iCre) expression in the mouse. Genesis 32:19-26.
39. Shoemaker LD, Arlotta P (2010) Untangling the cortex: Advances in understanding specification and differentiation of corticospinal motor neurons. Bioessays 32:197-206.
40. Simeone A, Acampora D, Pannese M, D'Esposito M, Stornaiuolo A, Gulisano M, Mallamaci A, Kastury K, Druck T, Huebner K (1994) Cloning and characterization of two members of the vertebrate Dlx gene family. Proc Natl Acad Sci U S A 91:2250-2254.
41. Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70-71.
42. Sousa VH, Miyoshi G, Hjerling-Leffler J, Karayannis T, Fishell G (2009) Characterization of Nkx6-2-derived neocortical interneuron lineages. Cereb Cortex 19 Suppl 1i1-i10.
43. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4.
44. Stanco A, Szekeres C, Patel N, Rao S, Campbell K, Kreidberg JA, Polleux F, Anton ES (2009) Netrin-1-alpha3beta1 integrin interactions regulate the migration of interneurons through the cortical marginal zone. Proc Natl Acad Sci U S A 106:7595-7600.
45. Stumm RK, Zhou C, Ara T, Lazarini F, Dubois-Dalcq M, Nagasawa T, Höllt V, Schulz S (2003) CXCR4 regulates interneuron migration in the developing neocortex. J Neurosci 23:5123-5130. (Pubitemid 36793240)
46. Taglialatela P, Soria JM, Caironi V, Moiana A, Bertuzzi S (2004) Compromised generation of GABAergic interneurons in the brains of Vax1-/- mice. Development 131:4239-4249.
47. Tanaka D, Nakaya Y, Yanagawa Y, Obata K, Murakami F (2003) Multimodal tangential migration of neocortical GABAergic neurons independent of GPI-anchored proteins. Development 130:5803-5813.
48. Tanaka DH, Maekawa K, Yanagawa Y, Obata K, Murakami F (2006) Multidirectional and multizonal tangential migration of GABAergic interneurons in the developing cerebral cortex. Development 133:2167-2176.
49. Tanaka DH, Yanagida M, Zhu Y, Mikami S, Nagasawa T, Miyazaki J, Yanagawa Y, Obata K, Murakami F (2009) Random walk behavior of migrating cortical interneurons in the marginal zone: time-lapse analysis in flat-mount cortex. J Neurosci 29:1300-1311.
50. Tiveron MC, Rossel M, Moepps B, Zhang YL, Seidenfaden R, Favor J, König N, Cremer H (2006) 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 26:13273-13278.
51. Tricoire L, Pelkey KA, Daw MI, Sousa VH, Miyoshi G, Jeffries B, Cauli B, Fishell G, McBain CJ (2010) Common origins of hippocampal Ivy and nitric oxide synthase expressing neurogliaform cells. J Neurosci 30:2165-2176.
52. Vucurovic K, Gallopin T, Ferezou I, Rancillac A, Chameau P, van Hooft JA, Geoffroy H, Monyer H, Rossier J, Vitalis T (2010) Serotonin 3A receptor subtype as an early and protracted marker of cortical interneuron subpopulations. Cereb Cortex. Advance online publication. Retrieved February 18, 2010. doi:10.1093/cercor/bhp310.
53. Wang Y, Dye CA, Sohal V, Long JE, Estrada RC, Roztocil T, Lufkin T, Deisseroth K, Baraban SC, Rubenstein JL (2010) Dlx5 and Dlx6 regulate the development of parvalbumin-expressing cortical interneurons. J Neurosci 30:5334-5345.
54. Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128:3759-3771.
55. Wonders CP, Anderson SA (2006) The origin and specification of cortical interneurons. Nat Rev Neurosci 7:687-696.
56. Wonders CP, Taylor L, Welagen J, Mbata IC, Xiang JZ, Anderson SA (2008) A spatial bias for the origins of interneuron subgroups within the medial ganglionic eminence. Dev Biol 314:127-136.
57. Xu Q, Tam M, Anderson SA (2008) Fate mapping Nkx2.1-lineage cells in the mouse telencephalon. J Comp Neurol 506:16-29.
58. Xu X, Roby KD, Callaway EM (2010) Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J Comp Neurol 518:389-404.
59. Yokota Y, Gashghaei HT, Han C, Watson H, Campbell KJ, Anton ES (2007) Radial glial dependent and independent dynamics of interneuronal migration in the developing cerebral cortex. PLoS One 2:e794.
60. Yozu M, Tabata H, Nakajima K (2005) The caudal migratory stream: a novel migratory stream of interneurons derived from the caudal ganglionic eminence in the developing mouse forebrain. J Neurosci 25:7268-7277.
61. Zhao Y, Flandin P, Long JE, Cuesta MD, Westphal H, Rubenstein JL (2008) Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants. J Comp Neurol 510:79-99.
62. Zimmer C, Lee J, Griveau A, Arber S, Pierani A, Garel S, Guillemot F (2010) Role of Fgf8 signalling in the specification of rostral Cajal-Retzius cells. Development 137:293-302.