A Radial Glia-Specific Role of RhoA in Double Cortex Formation

Neuron

Volumn 73, Issue 5, 2012, Pages 911-924

  Cappello, Silvia ^a   Böhringer, Christian R J ^a   Bergami, Matteo ^b   Conzelmann, Karl Klaus ^b   Ghanem, Alexander ^b   Tomassy, Giulio Srubek ^c   Arlotta, Paola ^c   Mainardi, Marco ^d   Allegra, Manuela ^d   Caleo, Matteo ^d   van Hengel, Jolanda ^e   Brakebusch, Cord ^f   Götz, Magdalena ^a,b  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c Harvard University   (United States)

^d CNR   (Italy)

^e GHENT UNIVERSITY   (Belgium)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL MIGRATION; COBBLESTONE LISSENCEPHALY; CONTROLLED STUDY; EMBRYO; GLIA CELL; MICROTUBULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIAL GLIA CELL; SUBCORTICAL HETEROTOPIA;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BROMODEOXYURIDINE; CELL MOVEMENT; CELL PROLIFERATION; CEREBRAL CORTEX; CLASSICAL LISSENCEPHALIES AND SUBCORTICAL BAND HETEROTOPIAS; DISEASE MODELS, ANIMAL; ELECTROPORATION; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; FEMALE; GAP-43 PROTEIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; PREGNANCY; RHOA GTP-BINDING PROTEIN; SILVER STAINING;

EID: 84858020309     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.12.030     Document Type: Article

References (74)

1. Beggs H.E., Schahin-Reed D., Zang K., Goebbels S., Nave K.A., Gorski J., Jones K.R., Sretavan D., Reichardt L.F. FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 2003, 40:501-514.
2. Belvindrah R., Graus-Porta D., Goebbels S., Nave K.A., Müller U. Beta1 integrins in radial glia but not in migrating neurons are essential for the formation of cell layers in the cerebral cortex. J. Neurosci. 2007, 27:13854-13865.
3. Berger J., Eckert S., Scardigli R., Guillemot F., Gruss P., Stoykova A. E1-Ngn2/Cre is a new line for regional activation of Cre recombinase in the developing CNS. Genesis 2004, 40:195-199.
4. Besson A., Gurian-West M., Schmidt A., Hall A., Roberts J.M. p27Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev. 2004, 18:862-876.
5. Bielas S., Higginbotham H., Koizumi H., Tanaka T., Gleeson J.G. Cortical neuronal migration mutants suggest separate but intersecting pathways. Annu. Rev. Cell Dev. Biol. 2004, 20:593-618.
6. Bilasy S.E., Satoh T., Ueda S., Wei P., Kanemura H., Aiba A., Terashima T., Kataoka T. Dorsal telencephalon-specific RA-GEF-1 knockout mice develop heterotopic cortical mass and commissural fiber defect. Eur. J. Neurosci. 2009, 29:1994-2008.
7. Cappello S., Attardo A., Wu X., Iwasato T., Itohara S., Wilsch-Bräuninger M., Eilken H.M., Rieger M.A., Schroeder T.T., Huttner W.B., et al. The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat. Neurosci. 2006, 9:1099-1107.
8. Chen L., Melendez J., Campbell K., Kuan C.Y., Zheng Y. Rac1 deficiency in the forebrain results in neural progenitor reduction and microcephaly. Dev. Biol. 2009, 325:162-170.
9. Coleman J.E., Nahmani M., Gavornik J.P., Haslinger R., Heynen A.J., Erisir A., Bear M.F. Rapid structural remodeling of thalamocortical synapses parallels experience-dependent functional plasticity in mouse primary visual cortex. J. Neurosci. 2010, 30:9670-9682.
10. Connelly J.T., Gautrot J.E., Trappmann B., Tan D.W., Donati G., Huck W.T., Watt F.M. Actin and serum response factor transduce physical cues from the microenvironment to regulate epidermal stem cell fate decisions. Nat. Cell Biol. 2010, 12:711-718.
11. Costell M., Gustafsson E., Aszódi A., Mörgelin M., Bloch W., Hunziker E., Addicks K., Timpl R., Fässler R. Perlecan maintains the integrity of cartilage and some basement membranes. J. Cell Biol. 1999, 147:1109-1122.
12. Creppe C., Malinouskaya L., Volvert M.L., Gillard M., Close P., Malaise O., Laguesse S., Cornez I., Rahmouni S., Ormenese S., et al. Elongator controls the migration and differentiation of cortical neurons through acetylation of alpha-tubulin. Cell 2009, 136:551-564.
13. Croquelois A., Giuliani F., Savary C., Kielar M., Amiot C., Schenk F., Welker E. Characterization of the HeCo mutant mouse: a new model of subcortical band heterotopia associated with seizures and behavioral deficits. Cereb. Cortex 2009, 19:563-575.
14. Englund C., Fink A., Lau C., Pham D., Daza R.A., Bulfone A., Kowalczyk T., Hevner R.F. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 2005, 25:247-251.
15. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
16. Feng Y., Chen M.H., Moskowitz I.P., Mendonza A.M., Vidali L., Nakamura F., Kwiatkowski D.J., Walsh C.A. Filamin A (FLNA) is required for cell-cell contact in vascular development and cardiac morphogenesis. Proc. Natl. Acad. Sci. USA 2006, 103:19836-19841.
17. Fietz S.A., Kelava I., Vogt J., Wilsch-Bräuninger M., Stenzel D., Fish J.L., Corbeil D., Riehn A., Distler W., Nitsch R., Huttner W.B. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat. Neurosci. 2010, 13:690-699.
18. Fitzgerald M.P., Covio M., Lee K.S. Disturbances in the positioning, proliferation and apoptosis of neural progenitors contribute to subcortical band heterotopia formation. Neuroscience 2011, 176:455-471.
19. Frotscher M. Role for Reelin in stabilizing cortical architecture. Trends Neurosci. 2010, 33:407-414.
20. Gandhi S.P., Yanagawa Y., Stryker M.P. Delayed plasticity of inhibitory neurons in developing visual cortex. Proc. Natl. Acad. Sci. USA 2008, 105:16797-16802.
21. Ge W., He F., Kim K.J., Blanchi B., Coskun V., Nguyen L., Wu X., Zhao J., Heng J.I., Martinowich K., et al. Coupling of cell migration with neurogenesis by proneural bHLH factors. Proc. Natl. Acad. Sci. USA 2006, 103:1319-1324.
22. Georges-Labouesse E., Mark M., Messaddeq N., Gansmüller A. Essential role of alpha 6 integrins in cortical and retinal lamination. Curr. Biol. 1998, 8:983-986.
23. Gleeson J.G., Allen K.M., Fox J.W., Lamperti E.D., Berkovic S., Scheffer I., Cooper E.C., Dobyns W.B., Minnerath S.R., Ross M.E., Walsh C.A. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 1998, 92:63-72.
24. Goebbels S., Bormuth I., Bode U., Hermanson O., Schwab M.H., Nave K.A. Genetic targeting of principal neurons in neocortex and hippocampus of NEX-Cre mice. Genesis 2006, 44:611-621.
25. Götz M. Doublecortin finds its place. Nat. Neurosci. 2003, 6:1245-1247.
26. Govek E.E., Newey S.E., Van Aelst L. The role of the Rho GTPases in neuronal development. Genes Dev. 2005, 19:1-49.
27. Guerrini R., Parrini E. Neuronal migration disorders. Neurobiol. Dis. 2010, 38:154-166.
28. Hall A., Lalli G. Rho and Ras GTPases in axon growth, guidance, and branching. Cold Spring Harb. Perspect. Biol. 2010, 2:a001818.
29. Hand R., Bortone D., Mattar P., Nguyen L., Heng J.I., Guerrier S., Boutt E., Peters E., Barnes A.P., Parras C., et al. Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 2005, 48:45-62.
30. Hansen D.V., Lui J.H., Parker P.R., Kriegstein A.R. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 2010, 464:554-561.
31. Haubst N., Georges-Labouesse E., De Arcangelis A., Mayer U., Götz M. Basement membrane attachment is dispensable for radial glial cell fate and for proliferation, but affects positioning of neuronal subtypes. Development 2006, 133:3245-3254.
32. Heasman S.J., Ridley A.J. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 2008, 9:690-701.
33. Heng J.I., Nguyen L., Castro D.S., Zimmer C., Wildner H., Armant O., Skowronska-Krawczyk D., Bedogni F., Matter J.M., Hevner R., Guillemot F. Neurogenin 2 controls cortical neuron migration through regulation of Rnd2. Nature 2008, 455:114-118.
34. Heng J.I., Chariot A., Nguyen L. Molecular layers underlying cytoskeletal remodelling during cortical development. Trends Neurosci. 2010, 33:38-47.
35. Herzog D., Loetscher P., van Hengel J., Knüsel S., Brakebusch C., Taylor V., Suter U., Relvas J.B. The small GTPase RhoA is required to maintain spinal cord neuroepithelium organization and the neural stem cell pool. J. Neurosci. 2011, 31:5120-5130.
36. Huang Z.J., Kirkwood A., Pizzorusso T., Porciatti V., Morales B., Bear M.F., Maffei L., Tonegawa S. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 1999, 98:739-755.
37. Iguchi T., Sakata K., Yoshizaki K., Tago K., Mizuno N., Itoh H. Orphan G protein-coupled receptor GPR56 regulates neural progenitor cell migration via a G alpha 12/13 and Rho pathway. J. Biol. Chem. 2008, 283:14469-14478.
38. Iwasato T., Nomura R., Ando R., Ikeda T., Tanaka M., Itohara S. Dorsal telencephalon-specific expression of Cre recombinase in PAC transgenic mice. Genesis 2004, 38:130-138.
39. Jackson B., Peyrollier K., Pedersen E., Basse A., Karlsson R., Wang Z., Lefever T., Ochsenbein A., Schmidt G., Aktories K., et al. RhoA is dispensable for skin development, but crucial for contraction and directed migration of keratinocytes. Mol. Biol. Cell 2011, 22:593-605.
40. Katayama K., Melendez J., Baumann J.M., Leslie J.R., Chauhan B.K., Nemkul N., Lang R.A., Kuan C.Y., Zheng Y., Yoshida Y. Loss of RhoA in neural progenitor cells causes the disruption of adherens junctions and hyperproliferation. Proc. Natl. Acad. Sci. USA 2011, 108:7607-7612.
41. Keays D.A., Tian G., Poirier K., Huang G.J., Siebold C., Cleak J., Oliver P.L., Fray M., Harvey R.J., Molnár Z., et al. Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell 2007, 128:45-57.
42. Kerjan G., Gleeson J.G. Genetic mechanisms underlying abnormal neuronal migration in classical lissencephaly. Trends Genet. 2007, 23:623-630.
43. Kholmanskikh S.S., Dobrin J.S., Wynshaw-Boris A., Letourneau P.C., Ross M.E. Disregulated RhoGTPases and actin cytoskeleton contribute to the migration defect in Lis1-deficient neurons. J. Neurosci. 2003, 23:8673-8681.
44. Kleinman H.K., Martin G.R. Matrigel: basement membrane matrix with biological activity. Semin. Cancer Biol. 2005, 15:378-386.
45. Kronenberg G., Gertz K., Baldinger T., Kirste I., Eckart S., Yildirim F., Ji S., Heuser I., Schröck H., Hörtnagl H., et al. Impact of actin filament stabilization on adult hippocampal and olfactory bulb neurogenesis. J. Neurosci. 2010, 30:3419-3431.
46. Lee K.S., Schottler F., Collins J.L., Lanzino G., Couture D., Rao A., Hiramatsu K., Goto Y., Hong S.C., Caner H., et al. A genetic animal model of human neocortical heterotopia associated with seizures. J. Neurosci. 1997, 17:6236-6242.
47. 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.
48. Leone D.P., Srinivasan K., Brakebusch C., McConnell S.K. The rho GTPase Rac1 is required for proliferation and survival of progenitors in the developing forebrain. Dev. Neurobiol. 2010, 70:659-678.
49. Li S., Jin Z., Koirala S., Bu L., Xu L., Hynes R.O., Walsh C.A., Corfas G., Piao X. GPR56 regulates pial basement membrane integrity and cortical lamination. J. Neurosci. 2008, 28:5817-5826.
50. Lien W.H., Klezovitch O., Fernandez T.E., Delrow J., Vasioukhin V. alphaE-catenin controls cerebral cortical size by regulating the hedgehog signaling pathway. Science 2006, 311:1609-1612.
51. Lodato S., Rouaux C., Quast K.B., Jantrachotechatchawan C., Studer M., Hensch T.K., Arlotta P. Excitatory projection neuron subtypes control the distribution of local inhibitory interneurons in the cerebral cortex. Neuron 2011, 69:763-779.
52. Machon O., van den Bout C.J., Backman M., Kemler R., Krauss S. Role of beta-catenin in the developing cortical and hippocampal neuroepithelium. Neuroscience 2003, 122:129-143.
53. Malatesta P., Hartfuss E., Götz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 2000, 127:5253-5263.
54. Moers A., Nürnberg A., Goebbels S., Wettschureck N., Offermanns S. Galpha12/Galpha13 deficiency causes localized overmigration of neurons in the developing cerebral and cerebellar cortices. Mol. Cell. Biol. 2008, 28:1480-1488.
55. Molyneaux B.J., Arlotta P., Menezes J.R., Macklis J.D. Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 2007, 8:427-437.
56. Munji R.N., Choe Y., Li G., Siegenthaler J.A., Pleasure S.J. Wnt signaling regulates neuronal differentiation of cortical intermediate progenitors. J. Neurosci. 2011, 31:1676-1687.
57. Nguyen L., Besson A., Heng J.I., Schuurmans C., Teboul L., Parras C., Philpott A., Roberts J.M., Guillemot F. p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev. 2006, 20:1511-1524.
58. Pacary E., Heng J., Azzarelli R., Riou P., Castro D., Lebel-Potter M., Parras C., Bell D.M., Ridley A.J., Parsons M., Guillemot F. Proneural transcription factors regulate different steps of cortical neuron migration through Rnd-mediated inhibition of RhoA signaling. Neuron 2011, 69:1069-1084.
59. Pinheiro E.M., Xie Z., Norovich A.L., Vidaki M., Tsai L.H., Gertler F.B. Lpd depletion reveals that SRF specifies radial versus tangential migration of pyramidal neurons. Nat. Cell Biol. 2011, 13:989-995.
60. Posern G., Sotiropoulos A., Treisman R. Mutant actins demonstrate a role for unpolymerized actin in control of transcription by serum response factor. Mol. Biol. Cell 2002, 13:4167-4178.
61. Radakovits R., Barros C.S., Belvindrah R., Patton B., Müller U. Regulation of radial glial survival by signals from the meninges. J. Neurosci. 2009, 29:7694-7705.
62. Reillo I., de Juan Romero C., Garcia-Cabezas M.A., Borrell V. A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb Cortex 2010, 10.1093/cercor/bhq238.
63. Reiner O., Carrozzo R., Shen Y., Wehnert M., Faustinella F., Dobyns W.B., Caskey C.T., Ledbetter D.H. Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 1993, 364:717-721.
64. Robertson S.P. Molecular pathology of filamin A: diverse phenotypes, many functions. Clin. Dysmorphol. 2004, 13:123-131.
65. Ross M.E., Walsh C.A. Human brain malformations and their lessons for neuronal migration. Annu. Rev. Neurosci. 2001, 24:1041-1070.
66. Saito T. In vivo electroporation in the embryonic mouse central nervous system. Nat. Protoc. 2006, 1:1552-1558.
67. Sarkisian M.R., Bartley C.M., Chi H., Nakamura F., Hashimoto-Torii K., Torii M., Flavell R.A., Rakic P. MEKK4 signaling regulates filamin expression and neuronal migration. Neuron 2006, 52:789-801.
68. Satz J.S., Ostendorf A.P., Hou S., Turner A., Kusano H., Lee J.C., Turk R., Nguyen H., Ross-Barta S.E., Westra S., et al. Distinct functions of glial and neuronal dystroglycan in the developing and adult mouse brain. J. Neurosci. 2010, 30:14560-14572.
69. Shitamukai A., Konno D., Matsuzaki F. Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors. J. Neurosci. 2011, 31:3683-3695.
70. Smart I.H., Dehay C., Giroud P., Berland M., Kennedy H. Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb. Cortex 2002, 12:37-53.
71. Vartiainen M.K., Guettler S., Larijani B., Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 2007, 316:1749-1752.
72. Vasioukhin V., Fuchs E. Actin dynamics and cell-cell adhesion in epithelia. Curr. Opin. Cell Biol. 2001, 13:76-84.
73. Wang X., Tsai J.W., LaMonica B., Kriegstein A.R. A new subtype of progenitor cell in the mouse embryonic neocortex. Nat. Neurosci. 2011, 14:555-561.
74. Wheeler A.P., Ridley A.J. Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility. Exp. Cell Res. 2004, 301:43-49.