Comprehensive spatiotemporal transcriptomic analyses of the ganglionic eminences demonstrate the uniqueness of its caudal subdivision

Molecular and Cellular Neuroscience

Volumn 37, Issue 4, 2008, Pages 845-856

  Willi Monnerat, Susan ^a   Migliavacca, Eugenia ^b,c,d   Surdez, Didier ^a   Delorenzi, Mauro ^b,c,d   Luthi Carter, Ruth ^a   Terskikh, Alexey V ^a,e  

^a EPFL   (Switzerland)

^b National Center of Competence in Research in Molecular Oncology   (Switzerland)

^c SWISS INST FOR EXP CANCER RESEARCH   (Switzerland)

^d SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^e BURNHAM INSTITUTE   (United States)

Author keywords

Cerebral cortex; Cortical interneurons; Ganglionic eminences; Gene expression profiling; Interneuronogenesis; Rat

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL SPECIFICITY; CONTROLLED STUDY; GABAERGIC SYSTEM; GANGLION; GENE EXPRESSION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT; TRANSCRIPTOMICS;

ANIMALS; CEREBRAL CORTEX; FEMALE; GENE EXPRESSION PROFILING; MEDIAN EMINENCE; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

RATTUS;

EID: 41149171604     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2008.01.009     Document Type: Article

References (80)

1. Alcantara S., de Lecea L., Del Rio J.A., Ferrer I., and Soriano E. Transient colocalization of parvalbumin and calbindin D28k in the postnatal cerebral cortex: evidence for a phenotypic shift in developing nonpyramidal neurons. Eur. J. Neurosci. 8 (1996) 1329-1339
2. Anderson K.D., and Reiner A. Immunohistochemical localization of DARPP-32 in striatal projection neurons and striatal interneurons: implications for the localization of D1-like dopamine receptors on different types of striatal neurons. Brain Res. 568 (1991) 235-243
3. Anderson S.A., Qiu M., Bulfone A., Eisenstat D.D., Meneses J., Pedersen R., and Rubenstein J.L. Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 19 (1997) 27-37
4. Anderson S.A., Marin O., Horn C., Jennings K., and Rubenstein J.L. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128 (2001) 353-363
5. Bach I., Carriere C., Ostendorff H.P., Andersen B., and Rosenfeld M.G. A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins. Genes Dev. 11 (1997) 1370-1380
6. Beissbarth T., and Speed T.P. GOstat: find statistically overrepresented Gene Ontologies within a group of genes. Bioinformatics 20 (2004) 1464-1465
7. Benjamini Y., and Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. JRSSB 57 (1995) 289-300
8. Bonaldo M.F., Lennon G., and Soares M.B. Normalization and subtraction: two approaches to facilitate gene discovery. Genome Res. 6 (1996) 791-806
9. Borrell V., and Marin O. Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling. Nat. Neurosci. 9 (2006) 1284-1293
10. Brazma A., Parkinson H., Sarkans U., Shojatalab M., Vilo J., Abeygunawardena N., Holloway E., Kapushesky M., Kemmeren P., Lara G.G., Oezcimen A., Rocca-Serra P., and Sansone S.A. ArrayExpress-a public repository for microarray gene expression data at the EBI. Nucleic Acids Res. 31 (2003) 68-71
11. Britton C.H., Mackey D.W., Esser V., Foster D.W., Burns D.K., Yarnall D.P., Froguel P., and McGarry J.D. Fine chromosome mapping of the genes for human liver and muscle carnitine palmitoyltransferase I (CPT1A and CPT1B). Genomics 40 (1997) 209-211
12. Bulfone A., Wang F., Hevner R., Anderson S., Cutforth T., Chen S., Meneses J., Pedersen R., Axel R., and Rubenstein J.L. An olfactory sensory map develops in the absence of normal projection neurons or GABAergic interneurons. Neuron 21 (1998) 1273-1282
13. Butt S.J., Fuccillo M., Nery S., Noctor S., Kriegstein A., Corbin J.G., and Fishell G. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48 (2005) 591-604
14. Chen F., Kook H., Milewski R., Gitler A.D., Lu M.M., Li J., Nazarian R., Schnepp R., Jen K., Biben C., Runke G., Mackay J.P., Novotny J., Schwartz R.J., Harvey R.P., Mullins M.C., and Epstein J.A. Hop is an unusual homeobox gene that modulates cardiac development. Cell 110 (2002) 713-723
15. Cheung K.K., Chan W.Y., and Burnstock G. Expression of P2X purinoceptors during rat brain development and their inhibitory role on motor axon outgrowth in neural tube explant cultures. Neuroscience 133 (2005) 937-945
16. Christophersen N.S., Gronborg M., Petersen T.N., Fjord-Larsen L., Jorgensen J.R., Juliusson B., Blom N., Rosenblad C., and Brundin P. Midbrain expression of Delta-like 1 homologue is regulated by GDNF and is associated with dopaminergic differentiation. Exp. Neurol. 204 (2007) 791-801
17. Cui L., Yu W.P., DeAizpurua H.J., Schmidli R.S., and Pallen C.J. Cloning and characterization of islet cell antigen-related protein-tyrosine phosphatase (PTP), a novel receptor-like PTP and autoantigen in insulin-dependent diabetes. J. Biol. Chem. 271 (1996) 24817-24823
18. Del Sal G., Ruaro M.E., Philipson L., and Schneider C. The growth arrest-specific gene, gas1, is involved in growth suppression. Cell 70 (1992) 595-607
19. Denaxa M., Chan C.H., Schachner M., Parnavelas J.G., and Karagogeos D. The adhesion molecule TAG-1 mediates the migration of cortical interneurons from the ganglionic eminence along the corticofugal fiber system. Development 128 (2001) 4635-4644
20. Eisen M.B., Spellman P.T., Brown P.O., and Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 14863-14868
21. Faedo A., Quinn J.C., Stoney P., Long J.E., Dye C., Zollo M., Rubenstein J.L., Price D.J., and Bulfone A. Identification and characterization of a novel transcript down-regulated in Dlx1/Dlx2 and up-regulated in Pax6 mutant telencephalon. Dev. Dyn. 231 (2004) 614-620
22. Feng L., Hatten M.E., and Heintz N. Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12 (1994) 895-908
23. Flames N., Pla R., Gelman D.M., Rubenstein J.L., Puelles L., and Marin O. Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J. Neurosci. 27 (2007) 9682-9695
24. Fleming A., Gerrelli D., Greene N.D., and Copp A.J. Mechanisms of normal and abnormal neurulation: evidence from embryo culture studies. Int. J. Dev. Biol. 41 (1997) 199-212
25. Fogarty M., Grist M., Gelman D., Marin O., Pachnis V., and Kessaris N. Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J. Neurosci. 27 (2007) 10935-10946
26. Fukuyama K., Yoshida M., Yamashita A., Deyama T., Baba M., Suzuki A., Mohri H., Ikezawa Z., Nakajima H., Hirai S., and Ohno S. MAPK upstream kinase (MUK)-binding inhibitory protein, a negative regulator of MUK/dual leucine zipper-bearing kinase/leucine zipper protein kinase. J. Biol. Chem. 275 (2000) 21247-21254
27. Gerfen C.R. The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci. 15 (1992) 133-139
28. Gerfen C.R., Engber T.M., Mahan L.C., Susel Z., Chase T.N., Monsma Jr. F.J., and Sibley D.R. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250 (1990) 1429-1432
29. Glasson S.S., Askew R., Sheppard B., Carito B., Blanchet T., Ma H.L., Flannery C.R., Peluso D., Kanki K., Yang Z., Majumdar M.K., and Morris E.A. Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis. Nature 434 (2005) 644-648
30. Graber M., and Burgunder J.M. Ontogeny of vasoactive intestinal peptide gene expression in rat brain. Anat. Embryol. (Berl) 194 (1996) 595-605
31. Graf E.R., Zhang X., Jin S.X., Linhoff M.W., and Craig A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119 (2004) 1013-1026
32. Grunder S., Geisler H.S., Rainier S., and Fink J.K. Acid-sensing ion channel (ASIC) 4 gene: physical mapping, genomic organisation, and evaluation as a candidate for paroxysmal dystonia. Eur. J. Hum. Genet. 9 (2001) 672-676
33. Hecht J.H., Weiner J.A., Post S.R., and Chun J. Ventricular zone gene-1 (vzg-1) encodes a lysophosphatidic acid receptor expressed in neurogenic regions of the developing cerebral cortex. J. Cell Biol. 135 (1996) 1071-1083
34. Holm P.C., Mader M.T., Haubst N., Wizenmann A., Sigvardsson M., and Gotz M. Loss- and gain-of-function analyses reveal targets of Pax6 in the developing mouse telencephalon. Mol. Cell. Neurosci. 34 (2007) 99-119
35. Horton S., Meredith A., Richardson J.A., and Johnson J.E. Correct coordination of neuronal differentiation events in ventral forebrain requires the bHLH factor MASH1. Mol. Cell. Neurosci. 14 (1999) 355-369
36. Jimenez D., Lopez-Mascaraque L.M., Valverde F., and De Carlos J.A. Tangential migration in neocortical development. Dev. Biol. 244 (2002) 155-169
37. Kalaydjieva L., Gresham D., Gooding R., Heather L., Baas F., de Jonge R., Blechschmidt K., Angelicheva D., Chandler D., Worsley P., Rosenthal A., King R.H., and Thomas P.K. N-myc downstream-regulated gene 1 is mutated in hereditary motor and sensory neuropathy-Lom. Am. J. Hum. Genet. 67 (2000) 47-58
38. Kang J.S., Mulieri P.J., Hu Y., Taliana L., and Krauss R.S. BOC, an Ig superfamily member, associates with CDO to positively regulate myogenic differentiation. Embo J. 21 (2002) 114-124
39. Kenwrick S., Watkins A., and De Angelis E. Neural cell recognition molecule L1: relating biological complexity to human disease mutations. Hum. Mol. Genet. 9 (2000) 879-886
40. Kessaris N., Fogarty M., Iannarelli P., Grist M., Wegner M., and Richardson W.D. Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat. Neurosci. 9 (2006) 173-179
41. Kile B.T., Viney E.M., Willson T.A., Brodnicki T.C., Cancilla M.R., Herlihy A.S., Croker B.A., Baca M., Nicola N.A., Hilton D.J., and Alexander W.S. Cloning and characterization of the genes encoding the ankyrin repeat and SOCS box-containing proteins Asb-1, Asb-2, Asb-3 and Asb-4. Gene 258 (2000) 31-41
42. Klar A., Baldassare M., and Jessell T.M. F-spondin: a gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite extension. Cell 69 (1992) 95-110
43. Kobayashi M., Toyama R., Takeda H., Dawid I.B., and Kawakami K. Overexpression of the forebrain-specific homeobox gene six3 induces rostral forebrain enlargement in zebrafish. Development 125 (1998) 2973-2982
44. Lavdas A.A., Grigoriou M., Pachnis V., and Parnavelas J.G. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 19 (1999) 7881-7888
45. Lee J.E., Hollenberg S.M., Snider L., Turner D.L., Lipnick N., and Weintraub H. Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268 (1995) 836-844
46. Ma L., and Tessier-Lavigne M. Dual branch-promoting and branch-repelling actions of Slit/Robo signaling on peripheral and central branches of developing sensory axons. J. Neurosci. 27 (2007) 6843-6851
47. Marin O., Anderson S.A., and Rubenstein J.L. Origin and molecular specification of striatal interneurons. J. Neurosci. 20 (2000) 6063-6076
48. Muzio L., and Mallamaci A. Emx1, emx2 and pax6 in specification, regionalization and arealization of the cerebral cortex. Cereb. Cortex 13 (2003) 641-647
49. Naeve G.S., Ramakrishnan M., Kramer R., Hevroni D., Citri Y., and Theill L.E. Neuritin: a gene induced by neural activity and neurotrophins that promotes neuritogenesis. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 2648-2653
50. Nery S., Wichterle H., and Fishell G. Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 128 (2001) 527-540
51. Nery S., Fishell G., and Corbin J.G. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat. Neurosci. 5 (2002) 1279-1287
52. Patwardhan S., Gashler A., Siegel M.G., Chang L.C., Joseph L.J., Shows T.B., Le Beau M.M., and Sukhatme V.P. EGR3, a novel member of the Egr family of genes encoding immediate-early transcription factors. Oncogene 6 (1991) 917-928
53. Pleasure S.J., Anderson S., Hevner R., Bagri A., Marin O., Lowenstein D.H., and Rubenstein J.L. Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28 (2000) 727-740
54. Polleux F., Whitford K.L., Dijkhuizen P.A., Vitalis T., and Ghosh A. Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling. Development 129 (2002) 3147-3160
55. Rask L., Anundi H., Fohlman J., and Peterson P.A. The complete amino acid sequence of human serum retinol-binding protein. Ups. J. Med. Sci. 92 (1987) 115-146
56. Salbaum J.M. Punc, a novel mouse gene of the immunoglobulin superfamily, is expressed predominantly in the developing nervous system. Mech. Dev. 71 (1998) 201-204
57. Saria A., Troger J., Kirchmair R., Fischer-Colbrie R., Hogue-Angeletti R., and Winkler H. Secretoneurin releases dopamine from rat striatal slices: a biological effect of a peptide derived from secretogranin II (chromogranin C). Neuroscience 54 (1993) 1-4
58. Smyth G.K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3 (2004) Article3
59. Stanton H., Rogerson F.M., East C.J., Golub S.B., Lawlor K.E., Meeker C.T., Little C.B., Last K., Farmer P.J., Campbell I.K., Fourie A.M., and Fosang A.J. ADAMTS5 is the major aggrecanase in mouse cartilage in vivo and in vitro. Nature 434 (2005) 648-652
60. Stenman J., Toresson H., and Campbell K. Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J. Neurosci. 23 (2003) 167-174
61. Strittmatter S.M., Fishman M.C., and Zhu X.P. Activated mutants of the alpha subunit of G(o) promote an increased number of neurites per cell. J. Neurosci. 14 (1994) 2327-2338
62. Stumm R.K., Zhou C., Ara T., Lazarini F., Dubois-Dalcq M., Nagasawa T., Hollt V., and Schulz S. CXCR4 regulates interneuron migration in the developing neocortex. J. Neurosci. 23 (2003) 5123-5130
63. Sussel L., Marin O., Kimura S., and 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 126 (1999) 3359-3370
64. Takiguchi-Hayashi K., Sekiguchi M., Ashigaki S., Takamatsu M., Hasegawa H., Suzuki-Migishima R., Yokoyama M., Nakanishi S., and Tanabe Y. Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles. J. Neurosci. 24 (2004) 2286-2295
65. Teufel A., Wong E.A., Mukhopadhyay M., Malik N., and Westphal H. FoxP4, a novel forkhead transcription factor. Biochim. Biophys. Acta 1627 (2003) 147-152
66. Toledo-Rodriguez M., Goodman P., Illic M., Wu C., and Markram H. Neuropeptide and calcium-binding protein gene expression profiles predict neuronal anatomical type in the juvenile rat. J. Physiol. 567 (2005) 401-413
67. Toresson H., Mata de Urquiza A., Fagerstrom C., Perlmann T., and Campbell K. Retinoids are produced by glia in the lateral ganglionic eminence and regulate striatal neuron differentiation. Development 126 (1999) 1317-1326
68. Tripodi M., Filosa A., Armentano M., and Studer M. The COUP-TF nuclear receptors regulate cell migration in the mammalian basal forebrain. Development 131 (2004) 6119-6129
69. Valcanis H., and Tan S.S. Layer specification of transplanted interneurons in developing mouse neocortex. J. Neurosci. 23 (2003) 5113-5122
70. Wang S.S., Tsai R.Y., and Reed R.R. The characterization of the Olf-1/EBF-like HLH transcription factor family: implications in olfactory gene regulation and neuronal development. J. Neurosci. 17 (1997) 4149-4158
71. Waters S.T., Wilson C.P., and Lewandoski M. Cloning and embryonic expression analysis of the mouse Gbx1 gene. Gene Expr. Patterns 3 (2003) 313-317
72. Werling U., and Schorle H. Transcription factor gene AP-2 gamma essential for early murine development. Mol. Cell. Biol. 22 (2002) 3149-3156
73. White J.A., Ramshaw H., Taimi M., Stangle W., Zhang A., Everingham S., Creighton S., Tam S.P., Jones G., and Petkovich M. Identification of the human cytochrome P450, P450RAI-2, which is predominantly expressed in the adult cerebellum and is responsible for all-trans-retinoic acid metabolism. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 6403-6408
74. Wichterle H., Garcia-Verdugo J.M., Herrera D.G., and Alvarez-Buylla A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat. Neurosci. 2 (1999) 461-466
75. Wichterle H., Turnbull D.H., Nery S., Fishell G., and Alvarez-Buylla A. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128 (2001) 3759-3771
76. Wonders C., and Anderson S.A. Cortical interneurons and their origins. Neuroscientist 11 (2005) 199-205
77. Wu Y., Sheng W., Chen L., Dong H., Lee V., Lu F., Wong C.S., Lu W.Y., and Yang B.B. Versican V1 isoform induces neuronal differentiation and promotes neurite outgrowth. Mol. Biol. Cell 15 (2004) 2093-2104
78. Xu Q., de la Cruz E., and Anderson S.A. Cortical interneuron fate determination: diverse sources for distinct subtypes?. Cereb. Cortex 13 (2003) 670-676
79. Xu Q., Cobos I., De La Cruz E., Rubenstein J.L., and Anderson S.A. Origins of cortical interneuron subtypes. J. Neurosci. 24 (2004) 2612-2622
80. Zerucha T., Stuhmer T., Hatch G., Park B.K., Long Q., Yu G., Gambarotta A., Schultz J.R., Rubenstein J.L., and 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. 20 (2000) 709-721