Ephrin-B1 controls the columnar distribution of cortical pyramidal neurons by restricting their tangential migration

Neuron

Volumn 79, Issue 6, 2013, Pages 1123-1135

  Dimidschstein, Jordane ^a   Passante, Lara ^a   Dufour, Audrey ^a   vandenAmeele, Jelle ^a,g   Tiberi, Luca ^a   Hrechdakian, Tatyana ^a   Adams, Ralf ^b,c   Klein, Rüdiger ^d   Lie, DieterChichung ^e   Jossin, Yves ^f   Vanderhaeghen, Pierre ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^e UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^f Fred Hutchinson Cancer Research Center   (United States)

^g GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN B1; EPHRIN RECEPTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; P REX1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL MIGRATION; CELL MOTILITY; CELL SPREADING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; FEMALE; GENE DISRUPTION; IN VIVO STUDY; MOLECULAR MECHANICS; MOUSE; NEURITE; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CARRIER PROTEINS; CELL ADHESION; CELL CYCLE PROTEINS; CELL MOVEMENT; CEREBRAL CORTEX; ELECTROPORATION; EMBRYO, MAMMALIAN; EPHRIN-B1; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; IMMUNOPRECIPITATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PREGNANCY; PYRAMIDAL CELLS; REPRESSOR PROTEINS;

EID: 84884248494     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.07.015     Document Type: Article

References (55)

1. Arvanitis D.N., Béhar A., Tryoen-Tóth P., Bush J.O., Jungas T., Vitale N., Davy A. Ephrin B1 maintains apical adhesion of neural progenitors. Development 2013, 140:2082-2092.
2. Batlle E., Wilkinson D.G. Molecular mechanisms of cell segregation and boundary formation in development and tumorigenesis. Cold Spring Harb. Perspect. Biol. 2012, 4:a008227.
3. 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.
4. Bochenek M.L., Dickinson S., Astin J.W., Adams R.H., Nobes C.D. Ephrin-B2 regulates endothelial cell morphology and motility independently of Eph-receptor binding. J.Cell Sci. 2010, 123:1235-1246.
5. Clandinin T.R., Feldheim D.A. Making a visual map: mechanisms and molecules. Curr. Opin. Neurobiol. 2009, 19:174-180.
6. Compagni A., Logan M., Klein R., Adams R.H. Control of skeletal patterning by ephrinB1-EphB interactions. Dev. Cell 2003, 5:217-230.
7. Cowan C.A., Henkemeyer M. The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals. Nature 2001, 413:174-179.
8. Dufour A., Seibt J., Passante L., Depaepe V., Ciossek T., Frisén J., Kullander K., Flanagan J.G., Polleux F., Vanderhaeghen P. Area specificity and topography of thalamocortical projections are controlled by ephrin/Eph genes. Neuron 2003, 39:453-465.
9. Egea J., Klein R. Bidirectional Eph-ephrin signaling during axon guidance. Trends Cell Biol. 2007, 17:230-238.
10. Flanagan J.G., Vanderhaeghen P. The ephrins and Eph receptors in neural development. Annu. Rev. Neurosci. 1998, 21:309-345.
11. Friocourt G., Kanatani S., Tabata H., Yozu M., Takahashi T., Antypa M., Raguenes O., Chelly J., Ferec C., Nakajima K., Parnavelas J.G. Cell-autonomous roles of ARX in cell proliferation and neuronal migration during corticogenesis. J.Neurosci. 2008, 28:5794-5805.
12. Fuentes P., Canovas J., Berndt F.A., Noctor S.C., Kukuljan M. CoREST/LSD1 control the development of pyramidal cortical neurons. Cereb. Cortex 2012, 22:1431-1441.
13. Genander M., Frisén J. Ephrins and Eph receptors in stem cells and cancer. Curr. Opin. Cell Biol. 2010, 22:611-616.
14. Guerrier S., Coutinho-Budd J., Sassa T., Gresset A., Jordan N.V., Chen K., Jin W.L., Frost A., Polleux F. The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell 2009, 138:990-1004.
15. Hajdo-Milasinović A., Ellenbroek S.I., van Es S., van der Vaart B., Collard J.G. Rac1 and Rac3 have opposing functions in cell adhesion and differentiation of neuronal cells. J.Cell Sci. 2007, 120:555-566.
16. Hajdo-Milasinović A., van der Kammen R.A., Moneva Z., Collard J.G. Rac3 inhibits adhesion and differentiation of neuronal cells by modifying GIT1 downstream signaling. J.Cell Sci. 2009, 122:2127-2136.
17. 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.
18. Huynh-Do U., Vindis C., Liu H., Cerretti D.P., McGrew J.T., Enriquez M., Chen J., Daniel T.O. Ephrin-B1 transduces signals to activate integrin-mediated migration, attachment and angiogenesis. J.Cell Sci. 2002, 115:3073-3081.
19. Ip J.P.K., Shi L., Chen Y., Itoh Y., Fu W.-Y., Betz A., Yung W.-H., Gotoh Y., Fu A.K.Y., Ip N.Y. α2-chimaerin controls neuronal migration and functioning of the cerebral cortex through CRMP-2. Nat. Neurosci. 2011, 15:39-47.
20. Jagasia R., Steib K., Englberger E., Herold S., Faus-Kessler T., Saxe M., Gage F.H., Song H., Lie D.C. GABA-cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus. J.Neurosci. 2009, 29:7966-7977.
21. Jessberger S., Zhao C., Toni N., Clemenson G.D., Li Y., Gage F.H. Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. J.Neurosci. 2007, 27:9400-9407.
22. Jørgensen C., Sherman A., Chen G.I., Pasculescu A., Poliakov A., Hsiung M., Larsen B., Wilkinson D.G., Linding R., Pawson T. Cell-specific information processing in segregating populations of Eph receptor ephrin-expressing cells. Science 2009, 326:1502-1509.
23. Jossin Y., Cooper J.A. Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex. Nat. Neurosci. 2011, 14:697-703.
24. Klein R. Bidirectional modulation of synaptic functions by Eph/ephrin signaling. Nat. Neurosci. 2009, 12:15-20.
25. Kriegstein A.R., Noctor S.C. Patterns of neuronal migration in the embryonic cortex. Trends Neurosci. 2004, 27:392-399.
26. Kwiatkowski A.V., Rubinson D.A., Dent E.W., Edward van Veen J., Leslie J.D., Zhang J., Mebane L.M., Philippar U., Pinheiro E.M., Burds A.A., et al. Ena/VASP Is Required for neuritogenesis in the developing cortex. Neuron 2007, 56:441-455.
27. Lallemand Y., Luria V., Haffner-Krausz R., Lonai P. Maternally expressed PGK-Cre transgene as a tool for early and uniform activation of the Cre site-specific recombinase. Transgenic Res. 1998, 7:105-112.
28. Li Y., Lu H., Cheng P.L., Ge S., Xu H., Shi S.H., Dan Y. Clonally related visual cortical neurons show similar stimulus feature selectivity. Nature 2012, 486:118-121.
29. LoTurco J.J., Bai J. The multipolar stage and disruptions in neuronal migration. Trends Neurosci. 2006, 29:407-413.
30. Marín O., Rubenstein J.L.R. Cell migration in the forebrain. Annu. Rev. Neurosci. 2003, 26:441-483.
31. Marín O., Valiente M., Ge X., Tsai L.H. Guiding neuronal cell migrations. Cold Spring Harb. Perspect. Biol. 2010, 2:a001834.
32. Noctor S.C., Martínez-Cerdeño V., Ivic L., Kriegstein A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 2004, 7:136-144.
33. North H.A., Zhao X., Kolk S.M., Clifford M.A., Ziskind D.M., Donoghue M.J. Promotion of proliferation in the developing cerebral cortex by EphA4 forward signaling. Development 2009, 136:2467-2476.
34. Ohshima T., Hirasawa M., Tabata H., Mutoh T., Adachi T., Suzuki H., Saruta K., Iwasato T., Itohara S., Hashimoto M., et al. Cdk5 is required for multipolar-to-bipolar transition during radial neuronal migration and proper dendrite development of pyramidal neurons in the cerebral cortex. Development 2007, 134:2273-2282.
35. Ohtsuki G., Nishiyama M., Yoshida T., Murakami T., Histed M., Lois C., Ohki K. Similarity of visual selectivity among clonally related neurons in visual cortex. Neuron 2012, 75:65-72.
36. 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.
37. 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.
38. Qiu R., Wang X., Davy A., Wu C., Murai K., Zhang H., Flanagan J.G., Soriano P., Lu Q. Regulation of neural progenitor cell state by ephrin-B. J.Cell Biol. 2008, 181:973-983.
39. Rakic P. Specification of cerebral cortical areas. Science 1988, 241:170-176.
40. Sentürk A., Pfennig S., Weiss A., Burk K., Acker-Palmer A. Ephrin Bs are essential components of the Reelin pathway to regulate neuronal migration. Nature 2011, 472:356-360.
41. Stuckmann I., Weigmann A., Shevchenko A., Mann M., Huttner W.B. Ephrin B1 is expressed on neuroepithelial cells in correlation with neocortical neurogenesis. J.Neurosci. 2001, 21:2726-2737.
42. Sun Y., Fei T., Yang T., Zhang F., Chen Y.G., Li H., Xu Z. The suppression of CRMP2 expression by bone morphogenetic protein (BMP)-SMAD gradient signaling controls multiple stages of neuronal development. J.Biol. Chem. 2010, 285:39039-39050.
43. Tabata H., Nakajima K. Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J.Neurosci. 2003, 23:9996-10001.
44. Tan S.S., Breen S. Radial mosaicism and tangential cell dispersion both contribute to mouse neocortical development. Nature 1993, 362:638-640.
45. Torii M., Hashimoto-Torii K., Levitt P., Rakic P. Integration of neuronal clones in the radial cortical columns by EphA and ephrin-A signalling. Nature 2009, 461:524-528.
46. Uchino S., Hirasawa T., Tabata H., Gonda Y., Waga C., Ondo Y., Nakajima K., Kohsaka S. Inhibition of N-methyl-D-aspartate receptor activity resulted in aberrant neuronal migration caused by delayed morphological development in the mouse neocortex. Neuroscience 2010, 169:609-618.
47. Valiente M., Ciceri G., Rico B., Marín O. Focal adhesion kinase modulates radial glia-dependent neuronal migration through connexin-26. J.Neurosci. 2011, 31:11678-11691.
48. Villar-Cerviño V., Molano-Mazón M., Catchpole T., Valdeolmillos M., Henkemeyer M., Martínez L.M., Borrell V., Marín O. Contact repulsion controls the dispersion and final distribution of Cajal-Retzius cells. Neuron 2013, 77:457-471.
49. Waters J.E., Astle M.V., Ooms L.M., Balamatsias D., Gurung R., Mitchell C.A. P-Rex1 - a multidomain protein that regulates neurite differentiation. J.Cell Sci. 2008, 121:2892-2903.
50. Westerlund N., Zdrojewska J., Padzik A., Komulainen E., Björkblom B., Rannikko E., Tararuk T., Garcia-Frigola C., Sandholm J., Nguyen L., et al. Phosphorylation of SCG10/stathmin-2 determines multipolar stage exit and neuronal migration rate. Nat. Neurosci. 2011, 14:305-313.
51. Xu N.J., Henkemeyer M. Ephrin-B3 reverse signaling through Grb4 and cytoskeletal regulators mediates axon pruning. Nat. Neurosci. 2009, 12:268-276.
52. Xu Z., Lai K.-O., Zhou H.-M., Lin S.-C., Ip N.Y. Ephrin-B1 reverse signaling activates JNK through a novel mechanism that is independent of tyrosine phosphorylation. J.Biol. Chem. 2003, 278:24767-24775.
53. Yoshizawa M., Kawauchi T., Sone M., Nishimura Y.V., Terao M., Chihama K., Nabeshima Y., Hoshino M. Involvement of a Rac activator, P-Rex1, in neurotrophin-derived signaling and neuronal migration. J.Neurosci. 2005, 25:4406-4419.
54. Yu Y.C., Bultje R.S., Wang X., Shi S.H. Specific synapses develop preferentially among sister excitatory neurons in the neocortex. Nature 2009, 458:501-504.
55. Yu Y.C., He S., Chen S., Fu Y., Brown K.N., Yao X.H., Ma J., Gao K.P., Sosinsky G.E., Huang K., Shi S.H. Preferential electrical coupling regulates neocortical lineage-dependent microcircuit assembly. Nature 2012, 486:113-117.