COUP-TFI Coordinates Cortical Patterning, Neurogenesis, and Laminar Fate and Modulates MAPK/ERK, AKT, and Beta-catenin Signaling

Overview

Journal Cereb Cortex

Publisher Oxford University Press

Specialty Neurology

Date 2008 Jan 1

PMID 18165280

Citations 78

Authors

Andrea Faedo

Giulio Srubek Tomassy

Youlin Ruan

Hannah Teichmann

Stefan Krauss

Samuel J Pleasure

Sophia Y Tsai

Ming-Jer Tsai

Michele Studer

John L R Rubenstein

Affiliations

Soon will be listed here.

Abstract

A major unsolved question in cortical development is how proliferation, neurogenesis, regional growth, regional identity, and laminar fate specification are coordinated. Here we provide evidence, using loss-of-function and gain-of-function manipulations, that the COUP-TFI orphan nuclear receptor promotes ventral cortical fate, promotes cell cycle exit and neural differentiation, regulates the balance of early- and late-born neurons, and regulates the balanced production of different types of layer V cortical projection neurons. We suggest that COUP-TFI controls these processes by repressing Mapk/Erk, Akt, and beta-catenin signaling.

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References

Kim A, Anderson S, Rubenstein J, Lowenstein D, Pleasure S . Pax-6 regulates expression of SFRP-2 and Wnt-7b in the developing CNS. J Neurosci. 2001; 21(5):RC132. PMC: 6762962. View

Qiu Y, Pereira F, Demayo F, Lydon J, Tsai S, Tsai M . Null mutation of mCOUP-TFI results in defects in morphogenesis of the glossopharyngeal ganglion, axonal projection, and arborization. Genes Dev. 1997; 11(15):1925-37. PMC: 316414. DOI: 10.1101/gad.11.15.1925. View

Iwata T, Chen L, Li C, Ovchinnikov D, Behringer R, Francomano C . A neonatal lethal mutation in FGFR3 uncouples proliferation and differentiation of growth plate chondrocytes in embryos. Hum Mol Genet. 2000; 9(11):1603-13. DOI: 10.1093/hmg/9.11.1603. View

Shinozaki K, Yoshida M, Nakamura M, Aizawa S, Suda Y . Emx1 and Emx2 cooperate in initial phase of archipallium development. Mech Dev. 2004; 121(5):475-89. DOI: 10.1016/j.mod.2004.03.013. View

Chen B, Schaevitz L, McConnell S . Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc Natl Acad Sci U S A. 2005; 102(47):17184-9. PMC: 1282569. DOI: 10.1073/pnas.0508732102. View

Theil T, Aydin S, Koch S, Grotewold L, Ruther U . Wnt and Bmp signalling cooperatively regulate graded Emx2 expression in the dorsal telencephalon. Development. 2002; 129(13):3045-54. DOI: 10.1242/dev.129.13.3045. View

Vaccarino , Schwartz , Raballo , Nilsen , Rhee , Zhou . Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis . Nat Neurosci. 1999; 2(9):848. DOI: 10.1038/12226. View

Sherr C, Kato J, Quelle D, Matsuoka M, Roussel M . D-type cyclins and their cyclin-dependent kinases: G1 phase integrators of the mitogenic response. Cold Spring Harb Symp Quant Biol. 1994; 59:11-9. DOI: 10.1101/sqb.1994.059.01.004. View

Bishop K, Garel S, Nakagawa Y, Rubenstein J, OLeary D . Emx1 and Emx2 cooperate to regulate cortical size, lamination, neuronal differentiation, development of cortical efferents, and thalamocortical pathfinding. J Comp Neurol. 2003; 457(4):345-60. DOI: 10.1002/cne.10549. View

10.

Assimacopoulos S, Grove E, Ragsdale C . Identification of a Pax6-dependent epidermal growth factor family signaling source at the lateral edge of the embryonic cerebral cortex. J Neurosci. 2003; 23(16):6399-403. PMC: 6740631. View

11.

Englund C, Fink A, Lau C, Pham D, Daza R, Bulfone A . Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci. 2005; 25(1):247-51. PMC: 6725189. DOI: 10.1523/JNEUROSCI.2899-04.2005. View

12.

Muzio L, Di Benedetto B, DiBenedetto B, Stoykova A, Boncinelli E, Gruss P . Conversion of cerebral cortex into basal ganglia in Emx2(-/-) Pax6(Sey/Sey) double-mutant mice. Nat Neurosci. 2002; 5(8):737-45. DOI: 10.1038/nn892. View

13.

Ding Q, Xia W, Liu J, Yang J, Lee D, Xia J . Erk associates with and primes GSK-3beta for its inactivation resulting in upregulation of beta-catenin. Mol Cell. 2005; 19(2):159-70. DOI: 10.1016/j.molcel.2005.06.009. View

14.

Scardigli R, Baumer N, Gruss P, Guillemot F, Le Roux I . Direct and concentration-dependent regulation of the proneural gene Neurogenin2 by Pax6. Development. 2003; 130(14):3269-81. DOI: 10.1242/dev.00539. View

15.

Shimamura K, Rubenstein J . Inductive interactions direct early regionalization of the mouse forebrain. Development. 1997; 124(14):2709-18. DOI: 10.1242/dev.124.14.2709. View

16.

Allendoerfer K, Shelton D, SHOOTER E, Shatz C . Nerve growth factor receptor immunoreactivity is transiently associated with the subplate neurons of the mammalian cerebral cortex. Proc Natl Acad Sci U S A. 1990; 87(1):187-90. PMC: 53226. DOI: 10.1073/pnas.87.1.187. View

17.

Cholfin J, Rubenstein J . Patterning of frontal cortex subdivisions by Fgf17. Proc Natl Acad Sci U S A. 2007; 104(18):7652-7. PMC: 1863435. DOI: 10.1073/pnas.0702225104. View

18.

Chen J, Rasin M, Kwan K, Sestan N . Zfp312 is required for subcortical axonal projections and dendritic morphology of deep-layer pyramidal neurons of the cerebral cortex. Proc Natl Acad Sci U S A. 2005; 102(49):17792-7. PMC: 1308928. DOI: 10.1073/pnas.0509032102. View

19.

Ye W, Shimamura K, Rubenstein J, Hynes M, Rosenthal A . FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell. 1998; 93(5):755-66. DOI: 10.1016/s0092-8674(00)81437-3. View

20.

Mason I . Initiation to end point: the multiple roles of fibroblast growth factors in neural development. Nat Rev Neurosci. 2007; 8(8):583-96. DOI: 10.1038/nrn2189. View