Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex

Nature Neuroscience

Volumn 14, Issue 6, 2011, Pages 697-703

  Jossin, Yves ^a   Cooper, Jonathan A ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1 ANTITRYPSIN; CADHERIN; GUANOSINE TRIPHOSPHATASE; INCADRONIC ACID; PROTEIN CDC42; PROTEIN KINASE B; RAC1 PROTEIN; RAP1 PROTEIN; REELIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; LOCOMOTION; MOUSE; NEOCORTEX; NERVE CELL; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

ANIMALS; CADHERINS; CELL ADHESION MOLECULES, NEURONAL; CELL DIFFERENTIATION; CELL MOVEMENT; EXTRACELLULAR MATRIX PROTEINS; MICE; MICE, INBRED STRAINS; NEOCORTEX; NERVE TISSUE PROTEINS; NEURONS; RAP1 GTP-BINDING PROTEINS; SERINE ENDOPEPTIDASES;

EID: 79960843611     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.2816     Document Type: Article

References (50)

1. 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. 20, 593-618 (2004). (Pubitemid 39488651)
2. Noctor, S.C., Martinez-Cerdeno, V., Ivic, L. & Kriegstein, A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144 (2004). (Pubitemid 38129789)
3. Tabata, H. & Nakajima, K. Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J. Neurosci. 23, 9996-10001 (2003). (Pubitemid 37392545)
4. de Anda, F.C., Meletis, K., Ge, X., Rei, D. & Tsai, L.H. Centrosome motility is essential for initial axon formation in the neocortex. J. Neurosci. 30, 10391-10406 (2010).
5. Nadarajah, B., Brunstrom, J.E., Grutzendler, J., Wong, R.O. & Pearlman, A.L. Two modes of radial migration in early development of the cerebral cortex. Nat. Neurosci. 4, 143-150 (2001). (Pubitemid 32125258)
6. Chen, G. et al. Semaphorin-3A guides radial migration of cortical neurons during development. Nat. Neurosci. 11, 36-44 (2008).
7. Tsai, J.W., Chen, Y., Kriegstein, A.R. & Vallee, R.B. LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages. J. Cell Biol. 170, 935-945 (2005). (Pubitemid 41306293)
8. Park, H.O. & Bi, E. Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol. Mol. Biol. Rev. 71, 48-96 (2007). (Pubitemid 46456684)
9. Schwamborn, J.C. & Puschel, A.W. The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat. Neurosci. 7, 923-929 (2004). (Pubitemid 39129500)
10. Nelson, W.J. Regulation of cell-cell adhesion by the cadherin-catenin complex. Biochem. Soc. Trans. 36, 149-155 (2008). (Pubitemid 351570584)
11. Kooistra, M.R., Dube, N. & Bos, J.L. Rap1: a key regulator in cell-cell junction formation. J. Cell Sci. 120, 17-22 (2007). (Pubitemid 46206645)
12. Jossin, Y. Neuronal migration and the role of reelin during early development of the cerebral cortex. Mol. Neurobiol. 30, 225-251 (2004). (Pubitemid 41264548)
13. Gumbiner, B.M. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84, 345-357 (1996). (Pubitemid 26058560)
14. Rubinfeld, B. et al. Molecular cloning of a GTPase activating protein specific for the Krev-1 protein p21rap1. Cell 65, 1033-1042 (1991). (Pubitemid 121001691)
15. Nichols, A.J., Carney, L.H. & Olson, E.C. Comparison of slow and fast neocortical neuron migration using a new in vitro model. BMC Neurosci. 9, 50 (2008).
16. Bivona, T.G. et al. Rap1 up-regulation and activation on plasma membrane regulates T cell adhesion. J. Cell Biol. 164, 461-470 (2004). (Pubitemid 38174773)
17. Boettner, B. & Van Aelst, L. Control of cell adhesion dynamics by Rap1 signaling. Curr. Opin. Cell Biol. 21, 684-693 (2009).
18. Takai, Y. & Nakanishi, H. Nectin and afadin: novel organizers of intercellular junctions. J. Cell Sci. 116, 17-27 (2003). (Pubitemid 36113961)
19. Belvindrah, R., Graus-Porta, D., Goebbels, S., Nave, K.A. & Muller, 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. 27, 13854-13865 (2007). (Pubitemid 350278262)
20. Rieger, S., Senghaas, N., Walch, A. & Koster, R.W. Cadherin-2 controls directional chain migration of cerebellar granule neurons. PLoS Biol. 7, e1000240 (2009).
21. Taniguchi, H., Kawauchi, D., Nishida, K. & Murakami, F. Classic cadherins regulate tangential migration of precerebellar neurons in the caudal hindbrain. Development 133, 1923-1931 (2006). (Pubitemid 43881258)
22. Davis, M.A., Ireton, R.C. & Reynolds, A.B. A core function for p120-catenin in cadherin turnover. J. Cell Biol. 163, 525-534 (2003). (Pubitemid 37429866)
23. Kuroda, S. et al. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin-mediated cell-cell adhesion. Science 281, 832-835 (1998). (Pubitemid 28376045)
24. Grindstaff, K.K. et al. Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell 93, 731-740 (1998). (Pubitemid 28257580)
25. Arthur, W.T., Quilliam, L.A. & Cooper, J.A. Rap1 promotes cell spreading by localizing Rac guanine nucleotide exchange factors. J. Cell Biol. 167, 111-122 (2004). (Pubitemid 39363419)
26. Moskalenko, S. et al. The exocyst is a Ral effector complex. Nat. Cell Biol. 4, 66-72 (2002). (Pubitemid 34071982)
27. Kadowaki, M. et al. N-cadherin mediates cortical organization in the mouse brain. Dev. Biol. 304, 22-33 (2007). (Pubitemid 46420318)
28. Chen, X., Kojima, S., Borisy, G.G. & Green, K.J. p120 catenin associates with kinesin and facilitates the transport of cadherin-catenin complexes to intercellular junctions. J. Cell Biol. 163, 547-557 (2003). (Pubitemid 37429868)
29. Ballif, B.A. et al. Activation of a Dab1/CrkL/C3G/Rap1 pathway in Reelin-stimulated neurons. Curr. Biol. 14, 606-610 (2004). (Pubitemid 38458951)
30. Jossin, Y., Gui, L. & Goffinet, A.M. Processing of Reelin by embryonic neurons is important for function in tissue but not in dissociated cultured neurons. J. Neurosci. 27, 4243-4252 (2007). (Pubitemid 46640708)
31. Uchida, T. et al. Downregulation of functional Reelin receptors in projection neurons implies that primary Reelin action occurs at early/premigratory stages. J. Neurosci. 29, 10653-10662 (2009).
32. Morimura, T. & Ogawa, M. Relative importance of the tyrosine phosphorylation sites of Disabled-1 to the transmission of Reelin signaling. Brain Res. 1304, 26-37 (2009).
33. Simó, S., Jossin, Y. & Cooper, J.A. Cullin 5 regulates cortical layering by modulating the speed and duration of Dab1-dependent neuronal migration. J. Neurosci. 30, 5668-5676 (2010).
34. Rice, D.S. et al. Disabled-1 acts downstream of Reelin in a signaling pathway that controls laminar organization in the mammalian brain. Development 125, 3719-3729 (1998). (Pubitemid 28469972)
35. Arnaud, L., Ballif, B.A. & Cooper, J.A. Regulation of protein tyrosine kinase signaling by substrate degradation during brain development. Mol. Cell. Biol. 23, 9293-9302 (2003). (Pubitemid 37499816)
36. Beffert, U. et al. Reelin-mediated signaling locally regulates protein kinase B/Akt and glycogen synthase kinase 3beta. J. Biol. Chem. 277, 49958-49964 (2002). (Pubitemid 36014446)
37. Jossin, Y. & Goffinet, A.M. Reelin signals through phosphatidylinositol 3-kinase and Akt to control cortical development and through mTor to regulate dendritic growth. Mol. Cell. Biol. 27, 7113-7124 (2007). (Pubitemid 47549749)
38. Ogawa, M. et al. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14, 899-912 (1995).
39. Goffinet, A.M. An early development defect in the cerebral cortex of the reeler mouse. A morphological study leading to a hypothesis concerning the action of the mutant gene. Anat. Embryol. (Berl.) 157, 205-216 (1979). (Pubitemid 10192068)
40. Elias, L.A., Wang, D.D. & Kriegstein, A.R. Gap junction adhesion is necessary for radial migration in the neocortex. Nature 448, 901-907 (2007). (Pubitemid 47312775)
41. Kawauchi, T. et al. Rab GTPases-dependent endocytic pathways regulate neuronal migration and maturation through N-cadherin trafficking. Neuron 67, 588-602 (2010).
42. Takeichi, M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251, 1451-1455 (1991). (Pubitemid 121000430)
43. Zhang, J. et al. Cortical neural precursors inhibit their own differentiation via N-cadherin maintenance of beta-catenin signaling. Dev. Cell 18, 472-479 (2010).
44. Yang, X., Chrisman, H. & Weijer, C.J. PDGF signaling controls the migration of mesoderm cells during chick gastrulation by regulating N-cadherin expression. Development 135, 3521-3530 (2008).
45. Fulga, T.A. & Rorth, P. Invasive cell migration is initiated by guided growth of long cellular extensions. Nat. Cell Biol. 4, 715-719 (2002). (Pubitemid 34993709)
46. Franco, S.J., Martinez-Garay, I., Gil-Sanz, C., Harkins-Perry, S.R. & Muller, U. Reelin regulates cadherin function via Dab1/Rap1 to control neuronal migration and lamination in the neocortex. Neuron 69, 482-497 (2011).
47. Liu, C. et al. Ras is required for the cyclic AMP-dependent activation of Rap1 via Epac2. Mol. Cell. Biol. 28, 7109-7125 (2008).
48. Tabata, H. & Nakajima, K. Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103, 865-872 (2001). (Pubitemid 32289300)
49. Jossin, Y., Ogawa, M., Metin, C., Tissir, F. & Goffinet, A.M. Inhibition of SRC family kinases and non-classical protein kinases C induce a reeler-like malformation of cortical plate development. J. Neurosci. 23, 9953-9959 (2003). (Pubitemid 37371611)
50. Qin, Y., Capaldo, C., Gumbiner, B.M. & Macara, I.G. The mammalian Scribble polarity protein regulates epithelial cell adhesion and migration through E-cadherin. J. Cell Biol. 171, 1061-1071 (2005). (Pubitemid 41815837)