The Rb/E2F pathway modulates neurogenesis through direct regulation of the Dlx1/Dlx2 bigene cluster

Journal of Neuroscience

Volumn 32, Issue 24, 2012, Pages 8219-8230

  Ghanem, Noël ^a,b   Andrusiak, Matthew G ^a   Svoboda, Devon ^a   Al Lafi, Sawsan M ^b   Julian, Lisa M ^a   McClellan, Kelly A ^a   de Repentigny, Yves ^c   Kothary, Rashmi ^c   Ekker, Marc ^a   Blais, Alexandre ^a   Park, David S ^a   Slack, Ruth S ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

^c OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CASPASE 3; GLUTAMATE DECARBOXYLASE 67; MICROTUBULE ASSOCIATED PROTEIN 2; REELIN; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DLX1; TRANSCRIPTION FACTOR DLX2; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR E2F7; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL CYCLE REGULATION; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; ENHANCER REGION; FEMALE; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERNEURON; KNOCKOUT MOUSE; MALE; MOUSE; MUTAGENESIS; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ANIMALS; BRAIN; CELL COUNT; E2F TRANSCRIPTION FACTORS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; INTERNEURONS; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEUROGENESIS; PREGNANCY; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84862267380     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1344-12.2012     Document Type: Article

References (52)

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. Anderson SA, Marín O, Horn C, Jennings K, Rubenstein JL (2001) Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128:353-363.
4. Batista-Brito R, Close J, Machold R, Fishell G (2008) The distinct temporal origins of olfactory bulb interneuron subtypes. J Neurosci 28:3966-3975.
5. Blais A, Dynlacht BD (2007) E2F-associated chromatin modifiers and cell cycle control. Curr Opin Cell Biol 19:658-662.
6. Bulfone A, Kim HJ, Puelles L, Porteus MH, Grippo JF, Rubenstein JL (1993) The mouse Dlx-2 (Tes-1) gene is expressed in spatially restricted domains of the forebrain, face and limbs in midgestation mouse embryos. Mech Dev 40:129-140.
7. Burkhart DL, Sage J (2008) Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat Rev Cancer 8:671-682.
8. Callaghan DA, Dong L, Callaghan SM, Hou YX, Dagnino L, Slack RS (1999) Neural precursor cells differentiating in the absence of Rb exhibit delayed terminal mitosis and deregulated E2F 1 and 3 activity. Dev Biol 207:257-270.
9. Calo E, Quintero-Estades JA, Danielian PS, Nedelcu S, Berman SD, Lees JA (2010) Rb regulates fate choice and lineage commitment in vivo. Nature 466:1110-1114.
10. Chen D, Opavsky R, Pacal M, Tanimoto N, Wenzel P, Seeliger MW, Leone G, Bremner R (2007) Rb-mediated neuronal differentiation through cellcycle-independent regulation of E2f3a. PLoS Biol 5:e179.
11. Chen HZ, Tsai SY, Leone G (2009) Emerging roles of E2Fs in cancer: an exit from cell cycle control. Nat Rev Cancer 9:785-797.
12. Christensen J, Cloos P, Toftegaard U, Klinkenberg D, Bracken AP, Trinh E, Heeran M, Di Stefano L, Helin K (2005) Characterization of E2F8, a novel E2F-like cell-cycle regulated repressor of E2F-activated transcription. Nucleic Acids Res 33:5458-5470.
13. Dick F, Dyson N (2006) Diverse regulatory functions of the E2F family of transcription factors. In: Rb and tumorigenesis (Fanciulli M, ed), pp 59-72. Austin, TX: Landes Bioscience.
14. Di Stefano L, Jensen MR, Helin K (2003) E2F7, a novel E2F featuring DPindependent repression of a subset of E2F-regulated genes. EMBO J 22:6289-6298.
15. 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.
16. Farkas LM, Huttner WB (2008) The cell biology of neural stem and progenitor cells and its significance for their proliferation versus differentiation during mammalian brain development. Curr Opin Cell Biol 20:707-715.
17. Ferguson KL, Vanderluit JL, Hébert JM, McIntosh WC, Tibbo E, MacLaurin JG, Park DS, Wallace VA, Vooijs M, McConnell SK, Slack RS (2002) Telencephalon-specific Rb knockouts reveal enhanced neurogenesis, survival and abnormal cortical development. EMBO J 21:3337-3346.
18. Ferguson KL, McClellan KA, Vanderluit JL, McIntosh WC, Schuurmans C, Polleux F, Slack RS (2005) A cell-autonomous requirement for the cell cycle regulatory protein, Rb, in neuronal migration. EMBO J 24:4381-4391.
19. Frank CL, Tsai LH (2009) Alternative functions of core cell cycle regulators in neuronal migration, neuronal maturation, and synaptic plasticity. Neuron 62:312-326.
20. Freedman JA, Chang JT, Jakoi L, Nevins JR (2009) A combinatorial mechanism for determining the specificity of E2F activation and repression. Oncogene 28:2873-2881.
21. Ghanem N, Jarinova O, Amores A, Long Q, Hatch G, Park BK, Rubenstein JL, Ekker M (2003) Regulatory roles of conserved intergenic domains in vertebrate Dlx bigene clusters. Genome Res 13:533-543.
22. Ghanem N, Yu M, Long J, Hatch G, Rubenstein JL, EkkerM (2007) 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 27:5012-5022.
23. Hébert JM, McConnell SK (2000) Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev Biol 222:296-306.
24. Herrup K, Silver J (1994) Cortical development and topographic maps: patterns of cell dispersion in developing cerebral cortex. Curr Opin Neurobiol 4:108-111.
25. Huh MS, Parker MH, Scimè A, Parks R, Rudnicki MA (2004) Rb is required for progression through myogenic differentiation but not maintenance of terminal differentiation. J Cell Biol 166:865-876.
26. Lammens T, Li J, Leone G, De Veylder L (2009) Atypical E2Fs: new players in the E2F transcription factor family. Trends Cell Biol 19:111-118.
27. Liu JK, Ghattas I, Liu S, Chen S, Rubenstein JL (1997) Dlx genes encode DNA-binding proteins that are expressed in an overlapping and sequential pattern during basal ganglia differentiation. Dev Dyn 210:498-512.
28. Long JE, Garel S, Alvarez-Dolado M, Yoshikawa K, Osumi N, Alvarez-Buylla A, Rubenstein JL (2007) Dlx-dependent and-independent regulation of olfactory bulb interneuron differentiation. J Neurosci 27:3230-3243.
29. Long JE, Cobos I, Potter GB, Rubenstein JL (2009) Dlx1&2 and Mash1 transcription factors control MGE and CGE patterning and differentiation through parallel and overlapping pathways. Cereb Cortex 19 [Suppl 1]:i96-i106.
30. MacPherson D, Sage J, Kim T, Ho D, McLaughlin ME, Jacks T (2004) Cell type-specific effects of Rb deletion in the murine retina. Genes Dev 18: 1681-1694.
31. Marino S, Vooijs M, van Der Gulden H, Jonkers J, Berns A (2000) Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev 14:994-1004.
32. Marino S, Hoogervoorst D, Brandner S, Berns A (2003) Rb and p107 are required for normal cerebellar development and granule cell survival but not for Purkinje cell persistence. Development 130:3359-3368.
33. McClellan KA, Slack RS (2006) Novel functions for cell cycle genes in nervous system development. Cell Cycle 5:1506-1513.
34. McClellan KA, Slack RS (2007) Specific in vivo roles for E2Fs in differentiation and development. Cell Cycle 6:2917-2927.
35. McClellan KA, Ruzhynsky VA, Douda DN, Vanderluit JL, Ferguson KL, Chen D, Bremner R, Park DS, Leone G, Slack RS (2007) Unique requirement for Rb/E2F3 in neuronal migration: evidence for cell cycle-independent functions. Mol Cell Biol 27:4825-4843.
36. McConnell SK, Kaznowski CE (1991) Cell cycle dependence of laminar determination in developing neocortex. Science 254:282-285.
37. Nguyen L, Besson A, Roberts JM, Guillemot F (2006) Coupling cell cycle exit, neuronal differentiation and migration in cortical neurogenesis. Cell Cycle 5:2314-2318.
38. Panganiban G, Rubenstein JL (2002) Developmental functions of the Distal-less/Dlx homeobox genes. Development 129:4371-4386.
39. 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.
40. Pleasure SJ, Anderson S, Hevner R, Bagri A, Marin O, Lowenstein DH, Rubenstein JL (2000) Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28:727-740.
41. Poitras L, Ghanem N, Hatch G, EkkerM (2007) The proneural determinant MASH1 regulates forebrain Dlx1/2 expression through the I12b intergenic enhancer. Development 134:1755-1765.
42. Porteus MH, Bulfone A, Ciaranello RD, Rubenstein JL (1991) Isolation and characterization of a novel cDNA clone encoding a homeodomain that is developmentally regulated in the ventral forebrain. Neuron 7:221-229.
43. Potter GB, Petryniak MA, Shevchenko E, McKinsey GL, Ekker M, Rubenstein JL (2009) Generation of Cre-transgenic mice using Dlx1/Dlx2 enhancers and their characterization in GABAergic interneurons. Mol Cell Neurosci 40:167-186.
44. Stevaux O, Dimova DK, Ji JY, Moon NS, Frolov MV, Dyson NJ (2005) Retinoblastoma family 2 is required in vivo for the tissue-specific repression of dE2F2 target genes. Cell Cycle 4:1272-1280.
45. Stühmer T, Anderson SA, Ekker M, Rubenstein JL (2002) Ectopic expression of the Dlx genes induces glutamic acid decarboxylase and Dlx expression. Development 129:245-252.
46. Takahashi C, Bronson RT, Socolovsky M, Contreras B, Lee KY, Jacks T, Noda M, Kucherlapati R, Ewen ME (2003) Rb and N-ras function together to control differentiation in the mouse. Mol Cell Biol 23:5256-5268.
47. Thomas DM, Carty SA, Piscopo DM, Lee JS, Wang WF, Forrester WC, Hinds PW (2001) The retinoblastoma protein acts as a transcriptional coactivator required for osteogenic differentiation. Mol Cell 8:303-316.
48. Tomita K, Ishibashi M, Nakahara K, Ang SL, Nakanishi S, Guillemot F, Kageyama R (1996) Mammalian hairy and Enhancer of split homolog 1 regulates differentiation of retinal neurons and is essential for eye morphogenesis. Neuron 16:723-734.
49. Wallace VA, Raff MC (1999) Arole for Sonic hedgehog in axon-to-astrocyte signalling in the rodent optic nerve. Development 126:2901-2909.
50. Xu X, Bieda M, Jin VX, Rabinovich A, Oberley MJ, Green R, Farnham PJ (2007) A comprehensive ChIP-chip analysis of E2F1, E2F4, and E2F6 in normal and tumor cells reveals interchangeable roles of E2F family members. Genome Res 17:1550-1561.
51. Yee SP, Rigby PW (1993) The regulation of myogenin gene expression during the embryonic development of the mouse. Genes Dev 7:1277-1289.
52. Zerucha T, Stühmer T, Hatch G, Park BK, Long Q, Yu G, Gambarotta A, Schultz JR, Rubenstein JL, EkkerM (2000) 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 20:709-721.