Biochemical and functional characterisation of αPIX, a specific regulator of axonal and dendritic branching in hippocampal neurons

Biology of the Cell

Volumn 104, Issue 9, 2012, Pages 533-552

  Totaro, Antonio ^a   Tavano, Stefania ^a   Filosa, Giuseppe ^a   Gärtner, Annette ^b   Pennucci, Roberta ^a   Santambrogio, Paolo ^a   Bachi, Angela ^a   Dotti, Carlos G ^b,c   De Curtis, Ivan ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Axon; Branching; Cofilin; Dendrite; Neuronal development

Indexed keywords

ISOPROTEIN; PROTEIN; PROTEIN ALPHA PIX; PROTEIN BETA PIX; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN DEVELOPMENT; CELL STRUCTURE; CHEMICAL ANALYSIS; CONTROLLED STUDY; DENDRITE; EMBRYO; GENE EXPRESSION; GENE OVEREXPRESSION; HIPPOCAMPUS; MASS SPECTROMETRY; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE FIBER; NEURITE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT;

ANIMALS; AXONS; CELL DIFFERENTIATION; CELLS, CULTURED; DENDRITES; GTPASE-ACTIVATING PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HIPPOCAMPUS; MICE; NEURONS; RATS;

EID: 84865847837     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1111/boc.201100060     Document Type: Article

References (62)

1. Abe, H., Ohshima, S. and Obinata, T. (1989) A cofilin-like protein is involved in the regulation of actin assembly in developing skeletal muscle. J. Biochem. 106, 696-702
2. Acebes, A. and Ferrus, A. (2000) Cellular and molecular features of axon collaterals and dendrites. Trends Neurosci. 23, 557-565
3. Albertinazzi, C., Za, L., Paris, S. and de Curtis, I. (2003) ADP-ribosylation factor 6 and a functional PIX/p95-APP1 complex are required for Rac1B-mediated neurite outgrowth. Mol. Biol. Cell 14, 1295-1307
4. Bagrodia, S., Bailey, D., Lenard, Z., Hart, M., Guan, J.L., Premont, R.T., Taylor, S.J. and Cerione, R.A. (1999) A tyrosine-phosphorylated protein that binds to an important regulatory region on the cool family of p21-activated kinase-binding proteins. J. Biol. Chem. 274, 22393-22400
5. Banker, G.A. and Cowan, W.M. (1977) Rat hippocampal neurons in dispersed cell culture. Brain Res. 126, 397-342
6. Boda, B., Alberi, S., Nikonenko, I., Node-Langlois, R., Jourdain, P., Moosmayer, M., Parisi-Jourdain, L. and Muller, D. (2004) The mental retardation protein PAK3 contributes to synapse formation and plasticity in hippocampus. J. Neurosci. 24, 10816-10825
7. Brown, M.C., Cary, L.A., Jamieson, J.S., Cooper, J.A. and Turner, C.E. (2005) Src and FAK kinases cooperate to phosphorylate paxillin kinase linker, stimulate its focal adhesion localization, and regulate cell spreading and protrusiveness. Mol. Biol. Cell 16, 4316-4328
8. de Curtis, I. (2001) Cell migration: GAPs between membrane traffic and the cytoskeleton. EMBO Rep. 2, 277-281
9. Dent, E.W., Barnes, A.M., Tang, F. and Kalil, K. (2004) Netrin-1 and semaphorin 3A promote or inhibit cortical axon branching, respectively, by reorganization of the cytoskeleton. J. Neurosci. 24, 3002-3012
10. Di Cesare, A., Paris, S., Albertinazzi, C., Dariozzi, S., Andersen, J., Mann, M., Longhi, R. and de Curtis, I. (2000) p95-APP1 links membrane transport to Rac-mediated reorganization of actin. Nat. Cell Biol. 2, 521-530
11. Dotti, C.G., Sullivan, C.A. and Banker, G.A. (1988) The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8, 1454-1468
12. Frank, S.R. and Hansen, S.H. (2008) The PIX-GIT complex: a G protein signaling cassette in control of cell shape. Semin. Cell Dev. Biol. 19, 234-244
13. Gallo, G. and Letourneau, P.C. (1998) Localized sources of neurotrophins initiate axon collateral branching. J. Neurosci. 18, 5403-5414
14. Garvalov, B.K., Flynn, K.C., Neukirchen, D., Meyn, L., Teusch, N., Wu, X., Brakebusch, C., Bamburg, J. R. and Bradke, F. (2007) Cdc42 regulates cofilin during the establishment of neuronal polarity. J. Neurosci. 27, 13117-13129
15. Gavina, M., Za, L., Molteni, R., Pardi, R. and de Curtis, I. (2010) The GIT-PIX complexes regulate the chemotactic response of rat basophilic leukaemia cells. Biol. Cell 102, 231-244
16. Gualdoni, S., Albertinazzi, C., Corbetta, S., Valtorta, F. and de Curtis, I. (2007) Normal levels of Rac1 are important for dendritic but not axonal development in hippocampal neurons. Biol. Cell 99, 455-464
17. Hayashi, K., Ohshima, T., Hashimoto, M. and Mikoshiba, K. (2007) Pak1 regulates dendritic branching and spine formation. Dev. Neurobiol. 67, 655-669
18. Heckel, T., Czupalla, C., Expirto Santo, A.I., Anitei, M., Arantzazu Sanchez-Fernandez, M., Mosch, K., Krause, E. and Hoflack, B. (2009) Src-dependent repression of ARF6 is required to maintain podosome-rich sealing zones in bone-digesting osteoclasts. Proc. Natl. Acad. Sci. U. S. A. 106, 1451-1456
19. Im, Y.J., Kang, G.B., Lee, J.H., Park, K.R., Song, H.E., Kim, E., Song, W.K., Park, D. and Eom, S.H. (2010) Structural basis for asymmetric association of the betaPIX coiled coil and shank PDZ. J. Mol. Biol. 397, 457-466
20. Jacobs, T., Causeret, F., Nishimura, Y.V., Terao, M., Norman, A., Hoshino, M. and Nikolić, M. (2007) Localized activation of p21-activated kinase controls neuronal polarity and morphology. J. Neurosci. 27, 8604-8615
21. Kaech, S. and Banker, G. (2006) Culturing hippocampal neurons. Nat. Protoc. 1, 2406-2415
22. Kim, S., Kim, T., Lee, D., Park, S.H., Kim, H. and Park, D. (2000) Molecular cloning of neuronally expressed mouse betaPix isoforms. Biochem. Biophys. Res. Commun. 272, 721-725
23. Kim, S., Ko, J., Shin, H., Lee, J.R., Lim, C., Han, J.H., Altrock, W.D., Garner, C.C., Gundelfinger, E.D., Premont, R.T., Kaang, B.K. and Kim, E. (2003) The GIT family of proteins forms multimers and associates with the presynaptic cytomatrix protein Piccolo. J. Biol. Chem. 278, 6291-6300
24. Ko, J., Kim, S., Valtschanoff, J.G., Shin, H., Lee, J.R., Sheng, M., Premont, R.T., Weinberg, R.J. and Kim, E. (2003) Interaction between liprin-alpha and GIT1 is required for AMPA receptor targeting. J. Neurosci. 23, 1667-1677
25. Koh, C.G., Manser, E., Zhao, Z.S., Ng, C.P. and Lim, L. (2001) β1PIX, 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
26. Kohn, M., Steinbach, P., Hameister, H. and Kehrer-Sawatzki, H. (2004) A comparative expression analysis of four MRX genes regulating intracellular signalling via small GTPases. Eur. J. Hum. Genet. 12, 29--37
27. Kreis, P. and Barnier, J.V. (2009) PAK signalling in neuronal physiology. Cell Signal. 21, 384-393
28. 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. and 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
29. Kutsche, K. and Gal, A. (2001) The mouse Arhgef6 gene: cDNA sequence, expression analysis, and chromosome assignment. Cytogenet. Cell Genet. 95, 196-201
30. Manabe, R., Kovalenko, M., Webb, D.J., and Horwitz, A.R. (2002) GIT1 functions in a motile, multi-molecular signaling complex that regulates protrusive activity and cell migration. J. Cell Sci. 115, 1497-1510
31. Manser, E., Loo, T.H., Koh, C.G., Zhao, Z.S., Chen, X.Q., Tan, L., Tan, I., Leung, T. and Lim, L. (1998) PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell 1, 183-192
32. Menon, P., Deane, R., Sagare, A., Lane, S.M., Zarcone, T.J., O'Dell, M.R., Yan, C., Zlokovic, B.V. and Berk, B.C. (2010) Impaired spine formation and learning in GPCR kinase 2 interacting protein-1 (GIT1) knockout mice. Brain Res. 1317, 218-226
33. Meyer, M.Z., Déliot, N., Chasserot-Golaz, S., Premont, R.T., Bader, M.F. and Vitale, N. (2006) Regulation of neuroendocrine exocytosis by the ARF6 GTPase-activating protein GIT1. J. Biol. Chem. 281, 7919-7926
34. Missy, K., Hu, B., Schilling, K., Harenberg, A., Sakk, V., Kuchenbecker, K., Kutsche, K. and Fischer, K.D. (2008) αPIX Rho GTPase guanine nucleotide exchange factor regulates lymphocyte functions and antigen receptor signaling. Mol. Cell. Biol. 28, 3776-3789
35. Momboisse, F., Lonchamp, E., Calco, V., Ceridono, M., Vitale, N., Bader, M.F. and Gasman, S. (2009) BetaPIX-activated Rac1 stimulates the activation of phospholipase D, which is associated with exocytosis in neuroendocrine cells. J. Cell Sci. 122, 798-806
36. Moriyama, K., Lida, K. and Yahara, I. (1996) Phosphorylation of Ser-3 of cofilin regulates its essential function on actin. Genes Cells 1, 73-86
37. Ng, J., Nardine, T., Harms, M., Tzu, J., Goldstein, A., Sun, Y., Dietzl, G., Dickson, B.J. and Luo, L. (2002) Rac GTPases control axon growth, guidance and branching. Nature 416, 442-447
38. Nodé-Langlois, R., Muller, D. and Boda, B. (2006) Sequential implication of the mental retardation proteins ARHGEF6 and PAK3 in spine morphogenesis. J. Cell Sci. 119, 4986-4993
39. Paris, S., Longhi, R., Santambrogio, P. and de Curtis, I. (2003) Leucine-zipper-mediated homo- and hetero-dimerization of GIT family p95-ARF GTPase-activating protein, PIX-, paxillin-interacting proteins 1 and 2. Biochem. J. 372, 391-398
40. Park, E., Na, M., Choi, J., Kim, S., Lee, J.R., Yoon, J., Park, D., Sheng, M. and Kim, E. (2003) The Shank family of postsynaptic density proteins interacts with and promotes synaptic accumulation of the beta PIX guanine nucleotide exchange factor for Rac1 and Cdc42. J. Biol. Chem. 278, 19220-19229
41. Parnas, D., Haghighi, A.P., Fetter, R.D., Kim, S.W. and Goodman, C.S. (2001) Regulation of postsynaptic structure and protein localization by the Rho-type guanine nucleotide exchange factor dPix. Neuron 32, 415-424
42. Premont, R.T., Claing, A., Vitale, N., Perry, S.J. and Lefkowitz, R.J. (2000) The GIT family of ADP-ribosylation factor GTPase-activating proteins. Functional diversity of GIT2 through alternative splicing. J. Biol. Chem. 275, 22373-22380
43. Premont, R.T., Perry, S.J., Schmalzigaug, R., Roseman, J.T., Xing, Y. and Claing, A. (2004) The GIT/PIX complex: an oligomeric assembly of GIT family ARF GTPase-activating proteins and PIX family Rac1/Cdc42 guanine nucleotide exchange factors. Cell Signal. 16, 1001-1011
44. Ramakers, G.J., Wolfer, D., Rosenberger, G., Kuchenbecker, K., Kreienkamp, H.J., Prange-Kiel, J., Rune, G., Richter, K., Langnaese, K., Masneuf, S., Bösl, M.R., Fischer, K.D., Krugers, H.J., Lipp, H.P., van Galen, E. and Kutsche, K. (2012) Dysregulation of Rho GTPases in the {alpha}Pix/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
45. Rappsilber, J., Mann, M. and Ishihama, Y. (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896-1906
46. Rosenberger, G. and Kutsche, K. (2006) AlphaPIX and betaPIX and their role in focal adhesion formation. Eur. J. Cell Biol. 85, 265-274
47. Sabe, H., Onodera, Y., Mazaki, Y. and Hashimoto, S. (2006) ArfGAP family proteins in cell adhesion, migration and tumor invasion. Curr. Opin. Cell Biol. 18, 558-564
48. Saneyoshi, T., Wayman, G., Fortin, D., Davare, M., Hoshi, N., Nozaki, N., Natsume, T. and Soderling, T.R. (2008) Activity-dependent synaptogenesis: regulation by a CaM-kinase kinase/CaM-kinase I/betaPIX signaling complex. Neuron 57, 94-107
49. Sarmiere, P.D. and Bamburg, J.R. (2004) Regulation of the neuronal actin cytoskeleton by ADF/cofilin. J. Neurobiol. 58, 103-117
50. Schlenker, O. and Rittinger, K. (2009) Structures of dimeric GIT1 and trimeric beta-PIX and implications for GIT-PIX complex assembly. J. Mol. Biol. 386, 280-289
51. Schmalzigaug, R., Phee, H., Davidson, C.E., Weiss, A. and Premont, R.T. (2007) Differential expression of the ARF GAP genes GIT1 and GIT2 in mouse tissues. J. Histochem. Cytochem. 55, 1039-1048
52. Schmalzigaug, R., Rodriguiz, R.M., Bonner, P.E., Davidson, C.E., Wetsel, W.C. and Premont, R.T. (2009a) Impaired fear response in mice lacking GIT1. Neurosci. Lett. 458, 79-83
53. Schmalzigaug, R., Rodriguiz, R.M., Phillips, L.E., Davidson, C.E., Wetsel, W.C. and Premont, R.T. (2009b) Anxiety-like behaviors in mice lacking GIT2. Neurosci. Lett. 451, 156-161
54. Segura, I., Essmann, C.L., Weinges, S. and Acker-Palmer, A. (2007) Grb4 and GIT1 transduce ephrinB reverse signals modulating spine morphogenesis and synapse formation. Nat. Neurosci. 10, 301-310
55. Shevchenko, A., Wilm, M., Vorm, O. and Mann, M. (1996) Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
56. Sun, Y. and Bamji, S.X. (2011) β-Pix modulates actin-mediated recruitment of synaptic vesicles to synapses. J. Neurosci. 31, 17123-17133
57. Totaro, A., Paris, S., Asperti, C. and de Curtis, I. (2007) Identification of an intramolecular interaction important for the regulation of GIT1 functions. Mol. Biol. Cell 18, 5124-5138
58. Won, H., Mah, W., Kim, E., Kim, J.W., Hahm, E.K., Kim, M.H., Cho, S., Kim, J., Jang, H., Cho, S.C., Kim, B.N., Shin, M.S., Seo, J., Jeong, J., Choi, S.Y., Kim, D., Kang, C. and Kim, E. (2011) GIT1 is associated with ADHD in humans and ADHD-like behaviors in mice. Nat. Med. 17, 566--572
59. Za, L., Albertinazzi, C., Paris, S., Gagliani, M., Tacchetti, C. andde Curtis, I. (2006) BetaPIX controls cell motility and neurite extension by regulating the distribution of GIT1. J. Cell Sci. 119, 2654-2666
60. Zhang, H., Webb, D.J., Asmussen, H. andHorwitz, A.F. (2003) Synapse formation is regulated by the signaling adaptor GIT1. J. Cell Biol. 161, 131-142
61. Zhang, H., Webb, D.J., Asmussen, H., Niu, S. andHorwitz, A.F. (2005) A GIT1/PIX/Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC. J. Neurosci. 25, 3379-3388
62. Zhao, Z.S., Manser, E., Loo, T.H. and Lim, L. (2000) Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol. Cell. Biol. 20, 6354-6363