Reelin and the Cdc42/Rac1 guanine nucleotide exchange factor αPIX/Arhgef6 promote dendritic Golgi translocation in hippocampal neurons

European Journal of Neuroscience

Volumn 37, Issue 9, 2013, Pages 1404-1412

  Meseke, Maurice ^a   Rosenberger, Georg ^a   Förster, Eckart ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

PIX; Golgi apparatus; Radial migration; Reeler; Rho GTPase

Indexed keywords

ALPHA PIX PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN CDC42; RAC1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL ADHESION MOLECULES, NEURONAL; DENDRITES; EXTRACELLULAR MATRIX PROTEINS; GOLGI APPARATUS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HIPPOCAMPUS; MICE; MICE, NEUROLOGIC MUTANTS; NERVE TISSUE PROTEINS; RAC1 GTP-BINDING PROTEIN; RATS; RATS, WISTAR; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION;

EID: 84877613376     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12153     Document Type: Article

References (50)

1. Ballif, B.A., Arnaud, L., Arthur, W.T., Guris, D., Imamoto, A. & Cooper, J.A. (2004) Activation of a Dab1/CrkL/C3G/Rap1 pathway in Reelin-stimulated neurons. Curr. Biol., 14, 606-610.
2. Brewer, G.J. (1997) Isolation and culture of adult rat hippocampal neurons. J. Neurosci. Meth., 71, 143-155.
3. Chai, X., Förster, E., Zhao, S., Bock, H.H. & Frotscher, M. (2009) Reelin stabilizes the actin cytoskeleton of neuronal processes by inducing n-cofilin phosphorylation at serine3. J. Neurosci., 29, 288-299.
4. Chen, C., Wirth, A. & Ponimaskin, E. (2012) Cdc42: an important regulator of neuronal morphology. Int. J. Biochem. Cell Biol., 44, 447-451.
5. Chen, G., Sima, J., Jin, M., Wang, K.-Y., Xue, X.-J., Zheng, W., Ding, Y.-Q. & Yuan, X.-B. (2008) Semaphorin-3A guides radial migration of cortical neurons during development. Nat. Neurosci., 11, 36-44.
6. Chen, K., Ochalski, P.G., Tran, T.S., Sahir, N., Schubert, M., Pramatarova, A. & Howell, B.W. (2004) Interaction between Dab1 and CrkII is promoted by Reelin signaling. J. Cell Sci., 117, 4527-4536.
7. Chen, R.H., Corbalan-Garcia, S. & Bar-Sagi, D. (1997) The role of the PH domain in the signal-dependent membrane targeting of Sos. EMBO J., 16, 1351-1359.
8. Curran, T. & D'Arcangelo, G. (1998) Role of reelin in the control of brain development. Brain Res. Brain Res. Rev., 26, 285-294.
9. Daniels, R.H., Zenke, F.T. & Bokoch, G.M. (1999) αPIX stimulates p21-activated kinase activity through exchange factor-dependent and -independent mechanisms. J. Biol. Chem., 274, 6047-6050.
10. D'Arcangelo, G. (2005) The reeler mouse: anatomy of a mutant. Int. Rev. Neurobiol., 71, 383-417.
11. D'Arcangelo, G., Nakajima, K., Miyata, T., Ogawa, M., Mikoshiba, K. & Curran, T. (1997) Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody. J. Neurosci., 17, 23-31.
12. Egea, G., Lázaro-Diéguez, F. & Vilella, M. (2006) Actin dynamics at the Golgi complex in mammalian cells. Curr. Opin. Cell Biol., 18, 168-178.
13. Erickson, J.W. & Cerione, R.A. (2001) Multiple roles for Cdc42 in cell regulation. Curr. Opin. Cell Biol., 13, 153-157.
14. Förster, E., Tielsch, A., Saum, B., Weiss, K.H., 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. USA, 99, 13178-13183.
15. Franco, S.J., Martinez-Garay, I., Gil-Sanz, C., Harkins-Perry, S.R. & Müller, U. (2011) Reelin regulates cadherin function via Dab1/Rap1 to control neuronal migration and lamination in the neocortex. Neuron, 69, 482-497.
16. Frotscher, M. (1998) Cajal-Retzius cells, Reelin, and the formation of layers. Curr. Opin. Neurobiol., 8, 570-575.
17. Govek, E.E., Hatten, M.E. & Van Aelst, L. (2011) The role of Rho GTPase proteins in CNS neuronal migration. Dev. Neurobiol., 71, 528-553.
18. Hartfuss, E., Förster, E., Bock, H.H., Hack, M.A., Leprince, P., Luque, J.M., Herz, J., Frotscher, M. & Götz, M. (2003) Reelin signaling directly affects radial glia morphology and biochemical maturation. Development, 130, 4597-4609.
19. Hiesberger, T., Trommsdorff, M., Howell, B.W., Goffinet, A., Mumby, M.C., Cooper, J.A. & 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.
20. Horton, A.C., Racz, B., Monson, E.E., Lin, A.L., Weinberg, R.J. & Ehlers, M.D. (2005) Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron, 48, 757-771.
21. Jossin, Y. & Cooper, J.A. (2011) Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex. Nat. Neurosci., 14, 697-703.
22. Kholmanskikh, S.S., Koeller, H.B., Wynshaw-Boris, A., Gomez, T., Letourneau, P.C. & Ross, M.E. (2006) Calcium-dependent interaction of Lis1 with IQGAP1 and Cdc42 promotes neuronal motility. Nat. Neurosci., 9, 50-57.
23. Kodani, A., Kristensen, I., Huang, L. & Sutterlin, C. (2009) GM130-dependent control of Cdc42 activity at the Golgi regulates centrosome organization. Mol. Biol. Cell, 20, 1192-1200.
24. Koh, C.G., Manser, E., Zhao, Z.S., Ng, C.P. & Lim, L. (2001) Beta1PIX, the PAK-interacting exchange factor, requires localization via a coiled-coil region to promote microvillus-like structures and membrane ruffles. J. Cell Sci., 114, 4239-4251.
25. Kubo, K., Honda, T., Tomita, K., Sekine, K., Ishii, K., Uto, A., Kobayashi, K., Tabata, H. & Nakajima, K. (2010) Ectopic Reelin induces neuronal aggregation with a normal birthdate-dependent "inside-out" alignment in the developing neocortex. J. Neurosci., 30, 10953-10966.
26. Kutsche, K., Yntema, H., Brandt, A., Jantke, I., Nothwang, H.G., Orth, U., Boavida, M.G., David, D., Chelly, J., Fryns, J.P., Moraine, C., Ropers, H.H., Hamel, B.C., van Bokhoven, H. & Gal, A. (2000) Mutations in ARHGEF6, encoding a guanine nucleotide exchange factor for Rho GTPases, in patients with X-linked mental retardation. Nat. Genet., 26, 247-250.
27. Lam, C., Vergnolle, M.A., Thorpe, L., Woodman, P.G. & Allan, V.J. (2010) Functional interplay between LIS1, NDE1 and NDEL1 in dynein-dependent organelle positioning. J. Cell Sci., 123, 202-212.
28. Leemhuis, J. & Bock, H.H. (2011) Reelin modulates cytoskeletal organization by regulating Rho GTPases. Commun. Integr. Biol., 4, 254-257.
29. Leemhuis, J., Bouche, E., Frotscher, M., Henle, F., Hein, L., Herz, J., Meyer, D.K., Pichler, M., Roth, G., Schwan, C. & Bock, H.H. (2010) Reelin signals through apolipoprotein E receptor 2 and Cdc42 to increase growth cone motility and filopodia formation. J. Neurosci., 30, 14759-14772.
30. Manser, E., Loo, T.H., Koh, C.G., Zhao, Z.S., Chen, X.Q., Tan, L., Tan, I., Leung, T. & Lim, L. (1998) PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell, 1, 183-192.
31. Matsuki, T., Matthews, R.T., Cooper, J.A., van der Brug, M.P., Cookson, M.R., Hardy, J.A., Olson, E.C. & Howell, B.W. (2010) Reelin and stk25 have opposing roles in neuronal polarization and dendritic Golgi deployment. Cell, 143, 826-836.
32. Meseke, M., Cavus, E. & Förster, E. (2013) Reelin promotes microtubule dynamics in processes of developing neurons. Histochem. Cell Biol., 139, 283-297.
33. Mo, J., Lee, D., Hong, S., Han, S., Yeo, H., Sun, W., Choi, S., Kim, H. & Lee, H.W. (2012) Preso regulation of dendritic outgrowth through PI(4, 5)P2-dependent PDZ interaction with betaPIX. Eur. J. Neurosci., 36, 1960-1970.
34. Nadarajah, B. & Parnavelas, J.G. (2002) Modes of neuronal migration in the developing cerebral cortex. Nat. Rev. Neurosci., 3, 423-432.
35. Nichols, A.J. & Olson, E.C. (2010) Reelin promotes neuronal orientation and dendritogenesis during preplate splitting. Cereb. Cortex, 20, 2213-2223.
36. Niu, S., Renfro, A., Quattrocchi, C.C., Sheldon, M. & D'Arcangelo, G. (2004) Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron, 41, 71-84.
37. O'Dell, R.S., Ustine, C.J., Cameron, D.A., Lawless, S.M., Williams, R.M., Zipfel, W.R. & Olson, E.C. (2012) Layer 6 cortical neurons require Reelin-Dab1 signaling for cellular orientation, Golgi deployment, and directed neurite growth into the marginal zone. Neural Dev., 7, 25.
38. Pinto Lord, M.C. & Caviness, V.S. Jr. (1979) Determinants of cell shape and orientation: a comparative Golgi analysis of cell-axon interrelationships in the developing neocortex of normal and reeler mice. J. Comp. Neurol., 187, 49-69.
39. Ramakers, G.J., Wolfer, D., Rosenberger, G., Kuchenbecker, K., Kreienkamp, H.J., Prange-Kiel, J., Rune, G., Richter, K., Langnaese, K., Masneuf, S., Bosl, M.R., Fischer, K.D., Krugers, H.J., Lipp, H.P., van Galen, E. & Kutsche, K. (2012) Dysregulation of Rho GTPases in the alphaPIX/Arhgef6 mouse model of X-linked intellectual disability is paralleled by impaired structural and synaptic plasticity and cognitive deficits. Hum. Mol. Genet., 21, 268-286.
40. Rosenberger, G., Jantke, I., Gal, A. & Kutsche, K. (2003) Interaction of alphaPIX (ARHGEF6) with beta-parvin (PARVB) suggests an involvement of alphaPIX in integrin-mediated signaling. Hum. Mol. Genet., 12, 155-167.
41. Rosenberger, G., Gal, A. & Kutsche, K. (2005) AlphaPIX associates with calpain 4, the small subunit of calpain, and has a dual role in integrin-mediated cell spreading. J. Biol. Chem., 280, 6879-6889.
42. Rossman, K.L., Der, C.J. & Sondek, J. (2005) GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol., 6, 167-180.
43. Schneider, S., Gulacsi, A. & Hatten, M.E. (2011) Lrp12/Mig13a reveals changing patterns of preplate neuronal polarity during corticogenesis that are absent in reeler mutant mice. Cereb. Cortex, 21, 134-144.
44. Sekine, K., Kawauchi, T., Kubo, K., Honda, T., Herz, J., Hattori, M., Kinashi, T. & Nakajima, K. (2012) Reelin controls neuronal positioning by promoting cell-matrix adhesion via inside-out activation of integrin alpha5beta1. Neuron, 76, 353-369.
45. Tissir, F. & Goffinet, A.M. (2003) Reelin and brain development. Nat. Rev. Neurosci., 4, 496-505.
46. Totaro, A., Tavano, S., Filosa, G., Gärtner, A., Pennucci, R., Santambrogio, P., Bachi, A., Dotti, C.G. & de Curtis, I. (2012) Biochemical and functional characterisation of αPIX, a specific regulator of axonal and dendritic branching in hippocampal neurons. Biol. Cell, 104, 533-552.
47. Walter, J., Kern-Veits, B., Huf, J., Stolze, B. & Bonhoeffer, F. (1987) Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development, 101, 685-696.
48. Yabut, O., Renfro, A., Niu, S., Swann, J.W., Marin, O. & D'Arcangelo, G. (2007) Abnormal laminar position and dendrite development of interneurons in the reeler forebrain. Brain Res., 1140, 75-83.
49. Ye, B., Zhang, Y., Song, W., Younger, S.H., Jan, L.Y. & Jan, Y.N. (2007) Growing dendrites and axons differ in their reliance on the secretory pathway. Cell, 130, 717-729.
50. 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.