Reelin signals through apolipoprotein E receptor 2 and Cdc42 to increase growth cone motility and filopodia formation

Journal of Neuroscience

Volumn 30, Issue 44, 2010, Pages 14759-14772

  Leemhuis, Jost ^a   Bouché, Elisabeth ^a   Frotscher, Michael ^a   Henle, Frank ^a   Hein, Lutz ^a   Herz, Joachim ^a,b   Meyer, Dieter K ^a   Pichler, Marina ^a   Roth, Günter ^a   Schwan, Carsten ^a   Bock, Hans H ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E RECEPTOR 2; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; LIPOPROTEIN RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; PROTEIN APOER2; PROTEIN CDC42; PROTEIN DISABLED 1; REELIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRANCHING MORPHOGENESIS; CELL MIGRATION; CELL MOTILITY; CELL STRUCTURE; CELL VACUOLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; FILOPODIUM; GROWTH CONE; MOUSE; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; CDC42 GTP-BINDING PROTEIN; CELL ADHESION MOLECULES, NEURONAL; CELL MOVEMENT; CELLS, CULTURED; CEREBRAL CORTEX; EXTRACELLULAR MATRIX PROTEINS; GROWTH CONES; HEK293 CELLS; HUMANS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; ORGAN CULTURE TECHNIQUES; PHOSPHATIDYLINOSITOL 3-KINASES; PSEUDOPODIA; RATS; RECEPTORS, LIPOPROTEIN; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION;

EID: 78049514270     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4036-10.2010     Document Type: Article

References (85)

1. Arnaud L, Ballif BA, Förster E, Cooper JA (2003a) Fyn tyrosine kinase is a critical regulator of disabled-1 during brain development. Curr Biol 13:9-17. (Pubitemid 36080617)
2. Arnaud L, Ballif BA, Cooper JA (2003b) Regulation of protein tyrosine kinase signaling by substrate degradation during brain development. Mol Cell Biol 23:9293-9302.
3. Assadi AH, Zhang G, Beffert U, McNeil RS, Renfro AL, Niu S, Quattrocchi CC, Antalffy BA, Sheldon M, Armstrong DD, Wynshaw-Boris A, Herz J, D'Arcangelo G, Clark GD (2003) Interaction of reelin signaling and Lis1 in brain development. Nat Genet 35:270-276.
4. Ayala R, Shu T, Tsai LH (2007) Trekking across the brain: the journey of neuronal migration. Cell 128:29-43.
5. Ballif BA, Arnaud L, Arthur WT, Guris D, Imamoto A, Cooper JA (2004) Activation of a Dab1/CrkL/C3G/Rap1 pathway in Reelin-stimulated neurons. Curr Biol 14:606-610.
6. Beffert U, Morfini G, Bock HH, Reyna H, Brady ST, Herz J (2002) Reelin-mediated signaling locally regulates protein kinase B/Akt and glycogen synthase kinase 3beta. J Biol Chem 277:49958-49964.
7. Bock HH, Herz J (2003) Reelin activates SRC family tyrosine kinases in neurons. Curr Biol 13:18-26.
8. Bock HH, Jossin Y, May P, Bergner O, Herz J (2004) Apolipoprotein E receptors are required for reelin-induced proteasomal degradation of the neuronal adaptor protein disabled-1. J Biol Chem 279:33471-33479.
9. Borrell V, Del Río JA, Alcántara S, Derer M, Martínez A, D'Arcangelo G, Nakajima K, Mikoshiba K, Derer P, Curran T, Soriano E (1999) Reelin regulates the development and synaptogenesis of the layer-specific entorhino-hippocampal connections. J Neurosci 19:1345-1358.
10. Bothwell M, Giniger E (2000) Alzheimer's disease: neurodevelopment converges with neurodegeneration. Cell 102:271-273.
11. Bradke F, Dotti CG (1997) Neuronal polarity: vectorial cytoplasmic flow precedes axon formation. Neuron 19:1175-1186.
12. Cantrell DA (2001) Phosphoinositide 3-kinase signalling pathways. J Cell Sci 114:1439-1445.
13. Chai X, Förster E, Zhao S, Bock HH, Frotscher M (2009) Reelin stabilizes the actin cytoskeleton of neuronal processes by inducing n-cofilin phosphorylation at serine 3. J Neurosci 29:288-299.
14. Chen Y, Beffert U, Ertunc M, Tang TS, Kavalali ET, Bezprozvanny I, Herz J (2005) Reelin modulates NMDA receptor activity in cortical neurons. J Neurosci 25:8209-8216.
15. Cooper JA (2008) A mechanism for inside-out lamination in the neocortex. Trends Neurosci 31:113-119.
16. Dai F, Yusuf F, Farjah GH, Brand-Saberi B (2005) RNAi-induced targeted silencing of developmental control genes during chicken embryogenesis. Dev Biol 285:80-90.
17. D'Arcangelo G, Homayouni R, Keshvara L, Rice DS, Sheldon M, Curran T (1999) Reelin is a ligand for lipoprotein receptors. Neuron 24:471-479.
18. Deitch JS, Banker GA (1993) An electron microscopic analysis of hippocampal neurons developing in culture: early stages in the emergence of polarity. J Neurosci 13:4301-4315.
19. Delamarche E, Bernard A, Schmid H, Michel B, Biebuyck H (1997) Patterned delivery of immunoglobulins to surfaces using microfluidic networks. Science 276:779-781.
20. Dickson L, Finlayson K (2009) VPAC and PAC receptors: from ligands to function. Pharmacol Ther 121:294-316.
21. Egea G, Lázaro-Diéguez F, Vilella M (2006) Actin dynamics at the Golgi complex in mammalian cells. Curr Opin Cell Biol 18:168-178.
22. Endo M, Ohashi K, Sasaki Y, Goshima Y, Niwa R, Uemura T, Mizuno K (2003) Control of growth cone motility and morphology by LIM kinase and slingshot via phosphorylation and dephosphorylation of cofilin. J Neurosci 23:2527-2537.
23. Erickson JW, Zhang C, Kahn RA, Evans T, Cerione RA (1996) Mammalian Cdc42 is a brefeldin A-sensitive component of the Golgi apparatus. J Biol Chem 271:26850-26854.
24. Etienne-Manneville S, Hall A (2001) Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106:489-498.
25. Fatemi SH (2005) Reelin glycoprotein: structure, biology and roles in health and disease. Mol Psychiatry 10:251-257.
26. Feng L, Allen NS, Simo S, Cooper JA (2007) Cullin 5 regulates Dab1 protein levels and neuron positioning during cortical development. Genes Dev 21:2717-2730.
27. Förster E, Tielsch A, Saum B, Weiss KH, Johanssen C, Graus-Porta D, Müller U, Frotscher M (2002) Reelin, Disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc Natl Acad Sci U S A 99:13178-13183.
28. Förster E, Zhao S, Frotscher M (2006) Laminating the hippocampus. Nat Rev Neurosci 7:259-267.
29. Goold RG, Owen R, Gordon-Weeks PR (1999) Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J Cell Sci 112:3373-3384.
30. Govek EE, Newey SE, Van Aelst L (2005) The role of the Rho GTPases in neuronal development. Genes Dev 19:1-49.
31. Hack I, Bancila M, Loulier K, Carroll P, Cremer H (2002) Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nat Neurosci 5:939-945.
32. Hack I, Hellwig S, Junghans D, Brunne B, Bock HH, Zhao S, Frotscher M (2007) Divergent roles of ApoER2 and Vldlr in the migration of cortical neurons. Development 134:3883-3891.
33. Hall A (2005) Rho GTPases and the control of cell behaviour. Biochem Soc Trans 33:891-895.
34. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, Connelly PA (1996) Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. J Biol Chem 271:695-701.
35. Hatten ME (1999) Central nervous system neuronal migration. Annu Rev Neurosci 22:511-539.
36. Hawkins PT, Anderson KE, Davidson K, Stephens LR (2006) Signalling through class I PI3Ks in mammalian cells. Biochem Soc Trans 34:647-662.
37. Heasman SJ, Ridley AJ (2008) Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9:690-701.
38. Henle F, Fischer C, Meyer DK, Leemhuis J (2006) Vasoactive intestinal peptide and PACAP38 control N-methyl-D-aspartic acid-induced dendrite motility by modifying the activities of Rho GTPases and phosphatidylinositol 3-kinases. J Biol Chem 281:24955-24969.
39. Herz J, Chen Y (2006) Reelin, lipoprotein receptors and synaptic plasticity. Nat Rev Neurosci 7:850-859.
40. Herz J, Goldstein JL, Strickland DK, Ho YK, Brown MS (1991) 39-kDa protein modulates binding of ligands to low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor. J Biol Chem 266:21232-21238.
41. Hiesberger T, Trommsdorff M, Howell BW, Goffinet A, Mumby MC, Cooper JA, Herz J (1999) Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24:481-489.
42. Horton AC, Ehlers MD (2003) Neuronal polarity and trafficking. Neuron 40:277-295.
43. Hotulainen P, Llano O, Smirnov S, Tanhuanpää K, Faix J, Rivera C, Lappalainen P (2009) Defining mechanisms of actin polymerization and depolymerization during dendritic spine morphogenesis. J Cell Biol 185:323-339.
44. Howell BW, Hawkes R, Soriano P, Cooper JA (1997) Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389:733-737.
45. Itoh RE, Kurokawa K, Ohba Y, Yoshizaki H, Mochizuki N, Matsuda M (2002) Activation of Rac and Cdc42 video imaged by fluorescent resonance energy transfer-based single-molecule probes in the membrane of living cells. Mol Cell Biol 22:6582-6591.
46. Jaffe AB, Hall A (2005) RHOGTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247-269.
47. Jossin Y, Gui L, Goffinet AM (2007) Processing of Reelin by embryonic neurons is important for function in tissue but not in dissociated cultured neurons. J Neurosci 27:4243-4252.
48. Kawauchi T, Hoshino M (2008) Molecular pathways regulating cytoskeletal organization and morphological changes in migrating neurons. Dev Neurosci 30:36-46.
49. Kholmanskikh SS, Koeller HB, Wynshaw-Boris A, Gomez T, Letourneau PC, Ross ME (2006) Calcium-dependent interaction of Lis1 with IQGAP1 and Cdc42 promotes neuronal motility. Nat Neurosci 9:50-57.
50. Kim WY, Zhou FQ, Zhou J, Yokota Y, Wang YM, Yoshimura T, Kaibuchi K, Woodgett JR, Anton ES, Snider WD (2006) Essential roles for GSK-3s and GSK-3-primed substrates in neurotrophin-induced and hippocampal axon growth. Neuron 52:981-996.
51. Konno D, Yoshimura S, Hori K, Maruoka H, Sobue K (2005) Involvement of the phosphatidylinositol 3-kinase/Rac1 and Cdc42 pathways in radial migration of cortical neurons. J Biol Chem 280:5082-5088.
52. Konur S, Ghosh A (2005) Calcium signaling and the control of dendritic development. Neuron 46:401-405.
53. Kuo G, Arnaud L, Kronstad-O'Brien P, Cooper JA (2005) Absence of Fyn and Src causes a Reeler-like phenotype. J Neurosci 25:8578-8586.
54. Leemhuis J, Boutillier S, Barth H, Feuerstein TJ, Brock C, Nürnberg B, Aktories K, Meyer DK (2004) Rho GTPases and phosphoinositide 3-kinase organize formation of branched dendrites. J Biol Chem 279:585-596.
55. Leemhuis J, Henle F, Meyer DK (2007) VIP induces the elongation of dendrites and axons in cultured hippocampal neurons: role of microtubules. Peptides 28:1700-1705.
56. Lewis DA, Levitt P (2002) Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci 25:409-432.
57. Luna A, Matas OB, Martínez-Menárguez JA, Mato E, Durán JM, Ballesta J, Way M, Egea G (2002) Regulation of protein transport from the Golgi complex to the endoplasmic reticulum by CDC42 and N-WASP. Mol Biol Cell 13:866-879.
58. Meyer DK, Fischer C, Becker U, Göttsching I, Boutillier S, Baermann C, Schmidt G, Klugbauer N, Leemhuis J (2005) Pituitary adenylyl cyclase-activating polypeptide 38 reduces astroglial proliferation by inhibiting the GTPase RhoA. J Biol Chem 280:25258-25266.
59. Meyer G, Feldman EL (2002) Signaling mechanisms that regulate actin-based motility processes in the nervous system. J Neurochem 83:490-503.
60. Nakamura T, Kurokawa K, Kiyokawa E, Matsuda M (2006) Analysis of the spatiotemporal activation of rho GTPases using Raichu probes. Methods Enzymol 406:315-332.
61. Ng J, Luo L (2004) Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron 44:779-793.
62. Niu S, Yabut O, D'Arcangelo G (2008) The Reelin signaling pathway promotes dendritic spine development in hippocampal neurons. J Neurosci 28:10339-10348.
63. Obermeier A, Ahmed S, Manser E, Yen SC, Hall C, Lim L (1998) PAK promotes morphological changes by acting upstream of Rac. EMBO J 17:4328-4339.
64. Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamoto H, Mikoshiba K (1995) The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14:899-912.
65. Pelish HE, Peterson JR, Salvarezza SB, Rodriguez-Boulan E, Chen JL, Stamnes M, Macia E, Feng Y, Shair MD, Kirchhausen T (2006) Secramine inhibits Cdc42-dependent functions in cells and Cdc42 activation in vitro. Nat Chem Biol 2:39-46.
66. Peterson JR, Bickford LC, Morgan D, Kim AS, Ouerfelli O, Kirschner MW, Rosen MK (2004) Chemical inhibition of N-WASP by stabilization of a native autoinhibited conformation. Nat Struct Mol Biol 11:747-755.
67. Pujadas L, Gruart A, Bosch C, Delgado L, Teixeira CM, Rossi D, de Lecea L, Martínez A, Delgado-García JM, Soriano E (2010) Reelin regulates postnatal neurogenesis and enhances spine hypertrophy and long-term potentiation. J Neurosci 30:4636-4649.
68. Rakic P (2006) A century of progress in corticoneurogenesis: from silver impregnation to genetic engineering. Cereb Cortex 16:i3-i17.
69. Ridley AJ (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16:522-529.
70. Sakakibara A, Horwitz AF (2006) Mechanism of polarized protrusion formation on neuronal precursors migrating in the developing chicken cerebellum. J Cell Sci 119:3583-3592.
71. Schaar BT, McConnell SK (2005) Cytoskeletal coordination during neuronal migration. Proc Natl Acad Sci U S A 102:13652-13657.
72. Shi SH, Jan LY, Jan YN (2003) Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112:63-75.
73. Solecki DJ, Govek EE, Hatten ME (2006) mPar6α controls neuronal migration. J Neurosci 26:10624-10625.
74. Soriano E, Del Río JA (2005) The cells of Cajal-Retzius: still a mystery one century after. Neuron 46:389-394.
75. Stolt PC, Bock HH (2006) Modulation of lipoprotein receptor functions by intracellular adaptor proteins. Cell Signal 18:1560-1571.
76. Suetsugu S, Tezuka T, Morimura T, Hattori M, Mikoshiba K, Yamamoto T, Takenawa T (2004) Regulation of actin cytoskeleton by mDab1 through N-WASP and ubiquitination of mDab1. Biochem J 384:1-8.
77. Tissir F, Goffinet AM (2003) Reelin and brain development. Nat Rev Neurosci 4:496-505.
78. Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J (1999) Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97:689-701.
79. Uchida T, Baba A, Pérez-Martínez FJ, Hibi T, Miyata T, Luque JM, Nakajima K, Hattori M (2009) Downregulation of functional reelin receptors in projection neurons implies that primary Reelin action occurs at early/premigratory stages. J Neurosci 29:10653-10662.
80. Vaudry D, Falluel-Morel A, Bourgault S, Basille M, Burel D, Wurtz O, Fournier A, Chow BK, Hashimoto H, Galas L, Vaudry H (2009) Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev 61:283-357.
81. Waschek JA (2002) Multiple actions of pituitary adenylyl cyclase activating peptide in nervous system development and regeneration. Dev Neurosci 24:14-23.
82. Wymann MP, Marone R (2005) Phosphoinositide 3-kinase in disease: timing, location, and scaffolding. Curr Opin Cell Biol 17:141-149.
83. Yoshida M, Assimacopoulos S, Jones KR, Grove EA (2006) Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development 133:537-545.
84. Zhao S, Chai X, Förster E, Frotscher M (2004) Reelin is a positional signal for the lamination of dentate granule cells. Development 131:5117-5125.
85. Zhou P, Porcionatto M, Pilapil M, Chen Y, Choi Y, Tolias KF, Bikoff JB, Hong EJ, Greenberg ME, Segal RA (2007) Polarized signaling endosomes coordinate BDNF-induced chemotaxis of cerebellar precursors. Neuron 55:53-68.