Transcriptional regulation of enhancers active in protodomains of the developing cerebral cortex

Neuron

Volumn 82, Issue 5, 2014, Pages 989-1003

  Pattabiraman, Kartik ^a   Golonzhka, Olga ^a,b   Lindtner, Susan ^a   Nord, Alex S ^c   Taher, Leila ^d,e   Hoch, Renee ^a   Silberberg, Shanni N ^a   Zhang, Dongji ^a   Chen, Bin ^f   Zeng, HongKui ^g   Pennacchio, Len A ^c,h   Puelles, Luis ⁱ   Visel, Axel ^c,h,j   Rubenstein, John L R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Acetylon Pharmaceuticals   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e UNIVERSITY OF ROSTOCK   (Germany)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^h DOE JOINT GENOME INSTITUTE   (United States)

ⁱ UNIVERSITY OF MURCIA   (Spain)

^j UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR 2; CRE RECOMBINASE; GREEN FLUORESCENT PROTEIN; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PBX1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; BRAIN CORTEX; BRAIN DEVELOPMENT; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DORSAL PALLIUM; EMBRYO; ENHANCER REGION; FRONTAL CORTEX; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE MAPPING; HIPPOCAMPUS; IN VIVO STUDY; LATERAL PALLIUM; MEDIAL PALLIUM; MOUSE; NERVOUS SYSTEM FUNCTION; NEUROEPITHELIUM; NONHUMAN; PRIMORDIUM; PRIORITY JOURNAL; TRANSCRIPTION REGULATION;

ANIMALS; BINDING SITES; CEREBRAL CORTEX; COUP TRANSCRIPTION FACTOR I; ENHANCER ELEMENTS, GENETIC; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, TRANSGENIC; PAIRED BOX TRANSCRIPTION FACTORS; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84901843699     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.04.014     Document Type: Article

References (49)

1. Ahituv N., Zhu Y., Visel A., Holt A., Afzal V., Pennacchio L.A., Rubin E.M. Deletion of ultraconserved elements yields viable mice. PLoS Biol. 2007, 5:e234.
2. Armentano M., Chou S.J., Tomassy G.S., Leingärtner A., O'Leary D.D., Studer M. COUP-TFI regulates the balance of cortical patterning between frontal/motor and sensory areas. Nat. Neurosci. 2007, 10:1277-1286.
3. Bielle F., Griveau A., Narboux-Nême N., Vigneau S., Sigrist M., Arber S., Wassef M., Pierani A. Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat. Neurosci. 2005, 8:1002-1012.
4. Bishop K.M., Goudreau G., O'Leary D.D. Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science 2000, 288:344-349.
5. Borello U., Madhavan M., Vilinsky I., Faedo A., Pierani A., Rubenstein J., Campbell K. Sp8 and COUP-TF1 reciprocally regulate patterning and Fgf signaling in cortical progenitors. Cereb. Cortex. 2013, Published online January 10, 2013. 10.1093/cercor/bhs412.
6. Chizhikov V.V., Lindgren A.G., Mishima Y., Roberts R.W., Aldinger K.A., Miesegaes G.R., Currle D.S., Monuki E.S., Millen K.J. Lmx1a regulates fates and location of cells originating from the cerebellar rhombic lip and telencephalic cortical hem. Proc. Natl. Acad. Sci. USA 2010, 107:10725-10730.
7. Chou S.J., Perez-Garcia C.G., Kroll T.T., O'Leary D.D. Lhx2 specifies regional fate in Emx1 lineage of telencephalic progenitors generating cerebral cortex. Nat. Neurosci. 2009, 12:1381-1389.
8. Clowney E.J., LeGros M.A., Mosley C.P., Clowney F.G., Markenskoff-Papadimitriou E.C., Myllys M., Barnea G., Larabell C.A., Lomvardas S. Nuclear aggregation of olfactory receptor genes governs their monogenic expression. Cell 2012, 151:724-737.
9. Colasante G., Collombat P., Raimondi V., Bonanomi D., Ferrai C., Maira M., Yoshikawa K., Mansouri A., Valtorta F., Rubenstein J.L., 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.
10. Faedo A., Tomassy G.S., Ruan Y., Teichmann H., Krauss S., Pleasure S.J., Tsai S.Y., Tsai M.J., Studer M., Rubenstein J.L. COUP-TFI coordinates cortical patterning, neurogenesis, and laminar fate and modulates MAPK/ERK, AKT, and beta-catenin signaling. Cereb. Cortex 2008, 18:2117-2131.
11. Farah M.H., Olson J.M., Sucic H.B., Hume R.I., Tapscott S.J., Turner D.L. Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development 2000, 127:693-702.
12. 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.
13. Galceran J., Miyashita-Lin E.M., Devaney E., Rubenstein J.L., Grosschedl R. Hippocampus development and generation of dentate gyrus granule cells is regulated by LEF1. Development 2000, 127:469-482.
14. Garcia-Lopez R., Pombero A., Martinez S. Fate map of the chick embryo neural tube. Dev. Growth Differ. 2009, 51:145-165.
15. Ghanem N., Yu M., Long J., Hatch G., Rubenstein J.L., Ekker M. Distinct cis-regulatory elements from the Dlx1/Dlx2 locus mark different progenitor cell populations in the ganglionic eminences and different subtypes of adult cortical interneurons. J.Neurosci. 2007, 27:5012-5022.
16. Gorski J.A., Talley T., Qiu M., Puelles L., Rubenstein J.L., Jones K.R. Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J.Neurosci. 2002, 22:6309-6314.
17. Guo C., Eckler M.J., McKenna W.L., McKinsey G.L., Rubenstein J.L.R., Chen B. Fezf2 expression identifies a multipotent progenitor for neocortical projection neurons, astrocytes, and oligodendrocytes. Neuron 2013, 80:1167-1174.
18. Hayashi S., McMahon A.P. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev. Biol. 2002, 244:305-318.
19. Hébert J.M., McConnell S.K. Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev. Biol. 2000, 222:296-306.
20. Hirata T., Li P., Lanuza G.M., Cocas L.A., Huntsman M.M., Corbin J.G. Identification of distinct telencephalic progenitor pools for neuronal diversity in the amygdala. Nat. Neurosci. 2009, 12:141-149.
21. 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.
22. Kammandel B., Chowdhury K., Stoykova A., Aparicio S., Brenner S., Gruss P. Distinct cis-essential modules direct the time-space pattern of the Pax6 gene activity. Dev. Biol. 1999, 205:79-97.
23. Konno D., Iwashita M., Satoh Y., Momiyama A., Abe T., Kiyonari H., Matsuzaki F. The mammalian DM domain transcription factor Dmrta2 is required for early embryonic development of the cerebral cortex. PLoS ONE 2012, 7:e46577.
24. Lagha M., Bothma J.P., Levine M. Mechanisms of transcriptional precision in animal development. Trends Genet. 2012, 28:409-416.
25. Leone D.P., Srinivasan K., Chen B., Alcamo E., McConnell S.K. The determination of projection neuron identity in the developing cerebral cortex. Curr. Opin. Neurobiol. 2008, 18:28-35.
26. 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.
27. Mallamaci A., Stoykova A. Gene networks controlling early cerebral cortex arealization. Eur. J. Neurosci. 2006, 23:847-856.
28. Mangale V.S., Hirokawa K.E., Satyaki P.R., Gokulchandran N., Chikbire S., Subramanian L., Shetty A.S., Martynoga B., Paul J., Mai M.V., et al. Lhx2 selector activity specifies cortical identity and suppresses hippocampal organizer fate. Science 2008, 319:304-309.
29. McKenna W.L., Betancourt J., Larkin K.A., Abrams B., Guo C., Rubenstein J.L., Chen B. Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development. J.Neurosci. 2011, 31:549-564.
30. Nord A.S., Blow M.J., Attanasio C., Akiyama J.A., Holt A., Hosseini R., Phouanenavong S., Plajzer-Frick I., Shoukry M., Afzal V., et al. Rapid and pervasive changes in genome-wide enhancer usage during mammalian development. Cell 2013, 155:1521-1531.
31. O'Leary D.D.M., Stocker A.M., Zembrzycki A. Area patterning of the mammalian cortex. Patterning and Cell Type Specification in the Developing CNS and PNS: Comprehensive Developmental Neuroscience 2013, 61-86. Academic Press, San Diego. J. Rubenstein, P. Rakic (Eds.).
32. Perry M.W., Boettiger A.N., Levine M. Multiple enhancers ensure precision of gap gene-expression patterns in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 2011, 108:13570-13575.
33. Puelles L. Pallio-pallial tangential migrations and growth signaling: new scenario for cortical evolution?. Brain Behav. Evol. 2011, 78:108-127.
34. Puelles L. Development and evolution of the claustrum. The Claustrum: Structural, Functional, and Clinical Neuroscience 2014, 119-176. Academic Press, San Diego. J. Smythies, L. Edelstein, V.S. Ramachandran (Eds.).
35. Puelles L., Kuwana E., Puelles E., Bulfone A., Shimamura K., Keleher J., Smiga S., Rubenstein J.L.R. Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J.Comp. Neurol. 2000, 424:409-438.
36. Rakic P. Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 2009, 10:724-735.
37. Sahara S., Kawakami Y., Izpisua Belmonte J.C., O'Leary D.D. Sp8 exhibits reciprocal induction with Fgf8 but has an opposing effect on anterior-posterior cortical area patterning. Neural Dev. 2007, 2:10.
38. Sansom S.N., Griffiths D.S., Faedo A., Kleinjan D.J., Ruan Y., Smith J., van Heyningen V., Rubenstein J.L., Livesey F.J. The level of the transcription factor Pax6 is essential for controlling the balance between neural stem cell self-renewal and neurogenesis. PLoS Genet. 2009, 5:e1000511.
39. Saulnier A., Keruzore M., De Clercq S., Bar I., Moers V., Magnani D., Walcher T., Filippis C., Kricha S., Parlier D., et al. The doublesex homolog Dmrt5 is required for the development of the caudomedial cerebral cortex in mammals. Cereb. Cortex 2013, 23:2552-2567.
40. Shim S., Kwan K.Y., Li M., Lefebvre V., Sestan N. Cis-regulatory control of corticospinal system development and evolution. Nature 2012, 486:74-79.
41. Teissier A., Griveau A., Vigier L., Piolot T., Borello U., Pierani A. A novel transient glutamatergic population migrating from the pallial-subpallial boundary contributes to neocortical development. J.Neurosci. 2010, 30:10563-10574.
42. Theil T., Aydin S., Koch S., Grotewold L., Rüther U. Wnt and Bmp signalling cooperatively regulate graded Emx2 expression in the dorsal telencephalon. Development 2002, 129:3045-3054.
43. van den Bout C.J., Machon O., Røsok Ø., Backman M., Krauss S. The mouse enhancer element D6 directs Cre recombinase activity in the neocortex and the hippocampus. Mech. Dev. 2002, 110:179-182.
44. Visel A., Taher L., Girgis H., May D., Golonzhka O., Hoch R.V., McKinsey G.L., Pattabiraman K., Silberberg S.N., Blow M.J., et al. A high-resolution enhancer atlas of the developing telencephalon. Cell 2013, 152:895-908.
45. 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.
46. Waclaw R.R., Ehrman L.A., Pierani A., Campbell K. Developmental origin of the neuronal subtypes that comprise the amygdalar fear circuit in the mouse. J.Neurosci. 2010, 30:6944-6953.
47. Xie Q., Yang Y., Huang J., Ninkovic J., Walcher T., Wolf L., Vitenzon A., Zheng D., Götz M., Beebe D.C., et al. Pax6 interactions with chromatin and identification of its novel direct target genes in lens and forebrain. PLoS ONE 2013, 8:e54507.
48. Yoshida M., Assimacopoulos S., Jones K.R., Grove E.A. Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development 2006, 133:537-545.
49. Yun K., Potter S., Rubenstein J.L.R. Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 2001, 128:193-205.