Foxp2 regulates neuronal differentiation and neuronal subtype specification

Developmental Neurobiology

Volumn 74, Issue 7, 2014, Pages 723-738

  Chiu, Yi Chi ^a   Li, Ming Yang ^a   Liu, Yuan Hsuan ^b   Ding, Jing Ya ^b   Yu, Jenn Yah ^b   Wang, Tsu Wei ^a,b  

^a NATIONAL TAIWAN NORMAL UNIVERSITY   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

Forebrain; Foxp2; Neurogenesis; PDGF receptor; Shh

Indexed keywords

PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR FOXP2; FORKHEAD TRANSCRIPTION FACTOR; FOXP2 PROTEIN, MOUSE; REPRESSOR PROTEIN; SHH PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL FATE; CELL PROLIFERATION; CELL SPECIFICITY; CELL SURVIVAL; CELL TYPE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FOREBRAIN; GANGLION; INTERNEURON; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; INBRED MOUSE STRAIN; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL SURVIVAL; CELLS, CULTURED; EMBRYONIC STEM CELLS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; INTERNEURONS; MICE; MICE, INBRED STRAINS; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; OLIGODENDROGLIA; PROSENCEPHALON; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84902103855     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.22166     Document Type: Article

References (48)

1. Brown AS, Begg MD, Gravenstein S, Schaefer CA, Wyatt RJ, Bresnahan M, Babulas VP, Susser ES. 2004. Serologic evidence of prenatal influenza in the etiology of schizophrenia. Arch Gen Psychiatry 61:774-780.
2. 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.
3. Butt SJ, Sousa VH, Fuccillo MV, Hjerling-Leffler J, Miyoshi G, Kimura S, Fishell G. 2008. The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron 59:722-732.
4. Campbell P, Reep RL, Stoll ML, Ophir AG, Phelps SM. 2009. Conservation and diversity of Foxp2 expression in muroid rodents: Functional implications. J Comp Neurol 512:84-100.
5. Carlsson P, Mahlapuu M. 2002. Forkhead transcription factors: Key players in development and metabolism. Dev Biol 250:1-23.
6. Chedotal A, Rijli FM. 2009. Transcriptional regulation of tangential neuronal migration in the developing forebrain. Curr Opin Neurobiol 19:139-145.
7. Chung KH, Hart CC, Al-Bassam S, Avery A, Taylor J, Patel PD, Vojtek AB, Turner DL. 2006. Polycistronic RNA polymerase II expression vectors for RNA interference based on BIC/miR-155. Nucleic Acids Res 34:e53.
8. Enard W. 2011. FOXP2 and the role of cortico-basal ganglia circuits in speech and language evolution. Curr Opin Neurobiol 21:415-424.
9. Enard W, Gehre S, Hammerschmidt K, Holter SM, Blass T, Somel M, Bruckner MK, Schreiweis C, Winter C, Sohr R, Becker L, Wiebe V, Nickel B, Giger T, Muller U, Groszer M, Adler T, Aguilar A, Bolle I, Calzada-Wack J, Dalke C, Ehrhardt N, Favor J, Fuchs H, Gailus-Durner V, Hans W, Holzlwimmer G, Javaheri A, Kalaydjiev S, Kallnik M, Kling E, Kunder S, Mossbrugger I, Naton B, Racz I, Rathkolb B, Rozman J, Schrewe A, Busch DH, Graw J, Ivandic B, Klingenspor M, Klopstock T, Ollert M, Quintanilla-Martinez L, Schulz H, Wolf E, Wurst W, Zimmer A, Fisher SE, Morgenstern R, Arendt T, de Angelis MH, Fischer J, Schwarz J, Paabo S. 2009. A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell 137:961-971.
10. Erlandsson A, Enarsson M, Forsberg-Nilsson K. 2001. Immature neurons from CNS stem cells proliferate in response to platelet-derived growth factor. J Neurosci 21:3483-3491.
11. Evans AE, Kelly CM, Precious SV, Rosser AE. 2012. Molecular regulation of striatal development: A review. Anat Res Int 2012:106529.
12. Farah MH, Olson JM, Sucic HB, Hume RI, Tapscott SJ, Turner DL. 2000. Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development 127:693-702.
13. Ferland RJ, Cherry TJ, Preware PO, Morrisey EE, Walsh CA. 2003. Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J Comp Neurol 460:266-279.
14. Foster GA, Schultzberg M, Hokfelt T, Goldstein M, Hemmings HC Jr, Ouimet CC, Walaas SI, Greengard P. 1987. Development of a dopamine- and cyclic adenosine 3':5'-monophosphate-regulated phosphoprotein (DARPP-32) in the prenatal rat central nervous system, and its relationship to the arrival of presumptive dopaminergic innervation. J Neurosci 7:1994-2018.
15. Fuccillo M, Joyner AL, Fishell G. 2006. Morphogen to mitogen: The multiple roles of hedgehog signalling in vertebrate neural development. Nat Rev Neurosci 7:772-783.
16. Fujita E, Tanabe Y, Shiota A, Ueda M, Suwa K, Momoi MY, Momoi T. 2008. Ultrasonic vocalization impairment of Foxp2 (R552H) knockin mice related to speech-language disorder and abnormality of Purkinje cells. Proc Natl Acad Sci U S A 105:3117-3122.
17. Groszer M, Keays DA, Deacon RM, de Bono JP, Prasad-Mulcare S, Gaub S, Baum MG, French CA, Nicod J, Coventry JA, Enard W, Fray M, Brown SD, Nolan PM, Paabo S, Channon KM, Costa RM, Eilers J, Ehret G, Rawlins JN, Fisher SE. 2008. Impaired synaptic plasticity and motor learning in mice with a point mutation implicated in human speech deficits. Curr Biol 18:354-362.
18. Haesler S, Rochefort C, Georgi B, Licznerski P, Osten P, Scharff C. 2007. Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area X. PLoS Biol 5:e321.
19. Hisaoka T, Nakamura Y, Senba E, Morikawa Y. 2010. The forkhead transcription factors, Foxp1 and Foxp2, identify different subpopulations of projection neurons in the mouse cerebral cortex. Neuroscience 166:551-563.
20. Kita H, Kitai ST. 1988. Glutamate decarboxylase immunoreactive neurons in rat neostriatum: Their morphological types and populations. Brain Res 447:346-352.
21. Konopka G, Bomar JM, Winden K, Coppola G, Jonsson ZO, Gao F, Peng S, Preuss TM, Wohlschlegel JA, Geschwind DH. 2009. Human-specific transcriptional regulation of CNS development genes by FOXP2. Nature 462:213-217.
22. Konstantoulas CJ, Parmar M, Li M. 2010. FoxP1 promotes midbrain identity in embryonic stem cell-derived dopamine neurons by regulating Pitx3. J Neurochem 113:836-847.
23. Lai CS, Fisher SE, Hurst JA, Vargha-Khadem F, Monaco AP. 2001. A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413:519-523.
24. Lee FH, Zai CC, Cordes SP, Roder JC, Wong AH. 2013. Abnormal interneuron development in disrupted-in-schizophrenia-1 L100P mutant mice. Mol Brain 6:20.
25. McBurney MW, Jones-Villeneuve EM, Edwards MK, Anderson PJ. 1982. Control of muscle and neuronal differentiation in a cultured embryonal carcinoma cell line. Nature 299:165-167.
26. Mednick SA, Machon RA, Huttunen MO, Bonett D. 1988. Adult schizophrenia following prenatal exposure to an influenza epidemic. Arch Gen Psychiatry 45:189-192.
27. Mohapel P, Frielingsdorf H, Haggblad J, Zachrisson O, Brundin P. 2005. Platelet-derived growth factor (PDGF-BB) and brain-derived neurotrophic factor (BDNF) induce striatal neurogenesis in adult rats with 6-hydroxydopamine lesions. Neuroscience 132:767-776.
28. Rochefort C, He X, Scotto-Lomassese S, Scharff C. 2007. Recruitment of FoxP2-expressing neurons to area X varies during song development. Dev Neurobiol 67:809-817.
29. Rousso DL, Pearson CA, Gaber ZB, Miquelajauregui A, Li S, Portera-Cailliau C, Morrisey EE, Novitch BG. 2012. Foxp-mediated suppression of N-cadherin regulates neuroepithelial character and progenitor maintenance in the CNS. Neuron 74:314-330.
30. Ruiz i Altaba A. 1998. Combinatorial Gli gene function in floor plate and neuronal inductions by Sonic hedgehog. Development 125:2203-2212.
31. Sasaki H, Hui C, Nakafuku M, Kondoh H. 1997. A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 124:1313-1322.
32. Sasaki H, Nishizaki Y, Hui C, Nakafuku M, Kondoh H. 1999. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: Implication of Gli2 and Gli3 as primary mediators of Shh signaling. Development 126:3915-3924.
33. Schulz SB, Haesler S, Scharff C, Rochefort C. 2010. Knockdown of FoxP2 alters spine density in Area X of the zebra finch. Genes Brain Behav 9:732-740.
34. Shu W, Cho JY, Jiang Y, Zhang M, Weisz D, Elder GA, Schmeidler J, De Gasperi R, Sosa MA, Rabidou D, Santucci AC, Perl D, Morrisey E, Buxbaum JD. 2005. Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene. Proc Natl Acad Sci U S A 102:9643-9648.
35. Spiteri E, Konopka G, Coppola G, Bomar J, Oldham M, Ou J, Vernes SC, Fisher SE, Ren B, Geschwind DH. 2007. Identification of the transcriptional targets of FOXP2, a gene linked to speech and language, in developing human brain. Am J Hum Genet 81:1144-1157.
36. Sussel L, Marin O, Kimura S, Rubenstein JL. 1999. 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 126:3359-3370.
37. Takahashi K, Liu FC, Hirokawa K, Takahashi H. 2003. Expression of Foxp2, a gene involved in speech and language, in the developing and adult striatum. J Neurosci Res 73:61-72.
38. Tolosa A, Sanjuan J, Dagnall AM, Molto MD, Herrero N, de Frutos R. 2010. FOXP2 gene and language impairment in schizophrenia: Association and epigenetic studies. BMC Med Genet 11:114.
39. Toresson H, Mata de Urquiza A, Fagerstrom C, Perlmann T, Campbell K. 1999. Retinoids are produced by glia in the lateral ganglionic eminence and regulate striatal neuron differentiation. Development 126:1317-1326.
40. Tsui D, Vessey JP, Tomita H, Kaplan DR, Miller FD. 2013. FoxP2 regulates neurogenesis during embryonic cortical development. J Neurosci 33:244-258.
41. Valenzuela CF, Kazlauskas A, Weiner JL. 1997. Roles of platelet-derived growth factor in the developing and mature nervous systems. Brain Res Brain Res Rev 24:77-89.
42. Vernes SC, Oliver PL, Spiteri E, Lockstone HE, Puliyadi R, Taylor JM, Ho J, Mombereau C, Brewer A, Lowy E, Nicod J, Groszer M, Baban D, Sahgal N, Cazier JB, Ragoussis J, Davies KE, Geschwind DH, Fisher SE. 2011. Foxp2 regulates gene networks implicated in neurite outgrowth in the developing brain. PLoS Genet 7:e1002145.
43. Vernes SC, Spiteri E, Nicod J, Groszer M, Taylor JM, Davies KE, Geschwind DH, Fisher SE. 2007. High-throughput analysis of promoter occupancy reveals direct neural targets of FOXP2, a gene mutated in speech and language disorders. Am J Hum Genet 81:1232-1250.
44. Williams BP, Park JK, Alberta JA, Muhlebach SG, Hwang GY, Roberts TM, Stiles CD. 1997. A PDGF-regulated immediate early gene response initiates neuronal differentiation in ventricular zone progenitor cells. Neuron 18:553-562.
45. Wonders CP, Anderson SA. 2006. The origin and specification of cortical interneurons. Nat Rev Neurosci 7:687-696.
46. Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA. 2004. Origins of cortical interneuron subtypes. J Neurosci 24:2612-2622.
47. Yu JY, Chung KH, Deo M, Thompson RC, Turner DL. 2008. MicroRNA miR-124 regulates neurite outgrowth during neuronal differentiation. Exp Cell Res 314:2618-2633.
48. Zhou B, Zhong Q, Minoo P, Li C, Ann DK, Frenkel B, Morrisey EE, Crandall ED, Borok Z. 2008. Foxp2 inhibits Nkx2.1-mediated transcription of SP-C via interactions with the Nkx2.1 homeodomain. Am J Respir Cell Mol Biol 38:750-758.