Brefeldin A-inhibited guanine exchange factor 2 regulates Filamin a phosphorylation and neuronal migration

Journal of Neuroscience

Volumn 32, Issue 36, 2012, Pages 12619-12629

  Zhang, Jingping ^a   Neal, Jason ^a   Lian, Gewei ^a   Shi, Bingxing ^b   Ferland, Russell J ^b,c   Sheen, Volney ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^c ALBANY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADP RIBOSYLATION FACTOR GUANINE EXCHANGE FACTOR 2; BREFELDIN A SENSITIVE SEC7 GUANINE EXCHANGE PROTEIN 2; FILAMIN A; GLIAL FIBRILLARY ACIDIC PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MYC PROTEIN; PAXILLIN; PHOSPHOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CYTOPLASM; EMBRYO; FEMALE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MOUSE; NERVE CELL; NEURAL STEM CELL; NONHUMAN; PERIVENTRICULAR HETEROTOPIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

ANIMALS; CELL MOVEMENT; CONTRACTILE PROTEINS; FEMALE; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; NEURONS; PHOSPHORYLATION;

EID: 84865763232     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1063-12.2012     Document Type: Article

References (44)

1. Achstetter T, Franzusoff A, Field C, Schekman R (1988) SEC7 encodes an unusual, high molecular weight protein required for membrane traffic from the yeast Golgi apparatus. J Biol Chem 263:11711-11717.
2. Charych EI, Yu W, Miralles CP, Serwanski DR, Li X, Rubio M, De Blas AL (2004) The brefeldin A-inhibited GDP/GTP exchange factor 2, a protein involved in vesicular trafficking, interacts with the beta subunits of the GABA receptors. J Neurochem 90:173-189.
3. D'Souza-Schorey C, Chavrier P (2006) ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7:347-358.
4. Faux CH, Parnavelas JG (2007) The role of intracellular calcium and RhoA in neuronal migration. Sci STKE 2007:pe62.
5. Feng Y, Chen MH, Moskowitz IP, Mendonza AM, Vidali L, Nakamura F, Kwiatkowski DJ, Walsh CA (2006) Filamin A (FLNA) is required for cell-cell contact in vascular development and cardiac morphogenesis. Proc Natl Acad Sci U S A 103:19836-19841.
6. Ferland RJ, Batiz LF, Neal J, Lian G, Bundock E, Lu J, Hsiao YC, Diamond R, Mei D, Banham AH, Brown PJ, Vanderburg CR, Joseph J, Hecht JL, Folkerth R, Guerrini R, Walsh CA, Rodriguez EM, Sheen VL (2009) Disruption of neural progenitors along the ventricular and subventricular zones in periventricular heterotopia. Hum Mol Genet 18:497-516.
7. Ferland RJ, Gaitanis JN, Apse K, Tantravahi U, Walsh CA, Sheen VL (2006) Periventricular nodular heterotopia and Williams syndrome. Am J Med Genet A 140:1305-1311.
8. Fox JW, Walsh CA (1999) Periventricular heterotopia and the genetics of neuronal migration in the cerebral cortex. Am J Hum Genet 65:19-24.
9. García E, Stracher A, Jay D (2006) Calcineurin dephosphorylates the C-terminal region of filamin in an important regulatory site: a possible mechanism for filamin mobilization and cell signaling. Arch Biochem Biophys 446:140-150.
10. Gérard-Blanluet M, Sheen V, Machinis K, Neal J, Apse K, Danan C, Sinico M, Brugières P, Mage K, Ratsimbazafy L, Elbez A, Janaud JC, Amselem S, Walsh C, Encha-Razavi F (2006) Bilateral periventricular heterotopias in an X-linked dominant transmission in a family with two affected males. Am J Med Genet A 140:1041-1046.
11. Gerwins P, Blank JL, Johnson GL (1997) Cloning of a novel mitogenactivated protein kinase kinase kinase, MEKK4, that selectively regulates the c-Jun amino terminal kinase pathway. J Biol Chem 272:8288-8295.
12. Grzmil P, Enkhbaatar Z, Gundsambuu B, Oidovsambuu O, Yalcin S, Wolf S, Engel W, Neesen J (2010) Early embryonic lethality in gene trap mice with disruption of the Arfgef2 gene. Int J Dev Biol 54:1259-1266.
13. He M, Zhang ZH, Guan CB, Xia D, Yuan XB (2010) Leading tip drives soma translocation via forward F-actin flow during neuronal migration. J Neurosci 30:10885-10898.
14. Jay D, García EJ, Lara JE, Medina MA, de la Luz Ibarra M (2000) Determination of a cAMP-dependent protein kinase phosphorylation site in the C-terminal region of human endothelial actin-binding protein. Arch Biochem Biophys 377:80-84.
15. Jay D, García EJ, de la Luz Ibarra M (2004) In situ determination of a PKA phosphorylation site in the C-terminal region of filamin. Mol Cell Biochem 260:49-53.
16. Jones HD, Moss J, Vaughan M (2005) BIG1 and BIG2, brefeldin A-inhibited guanine nucleotide-exchange factors for ADP-ribosylation factors. Methods Enzymol 404:174-184.
17. Jones KJ, Korb E, Kundel MA, Kochanek AR, Kabraji S, McEvoy M, Shin CY, Wells DG (2008) CPEB1 regulates beta-catenin mRNA translation and cell migration in astrocytes. Glia 56:1401-1413.
18. Letinic K, Sebastian R, Toomre D, Rakic P (2009) Exocyst is involved in polarized cell migration and cerebral cortical development. Proc Natl Acad Sci U S A 106:11342-11347.
19. Li H, Adamik R, Pacheco-Rodriguez G, Moss J, Vaughan M (2003) Protein kinase A-anchoring (AKAP) domains in brefeldin A-inhibited guanine nucleotide-exchange protein 2 (BIG2). Proc Natl Acad Sci USA100:1627-1632.
20. Lian G, Lu J, Hu J, Zhang J, Ferland R, Sheen V (2012) Filamin A regulates neural progenitor proliferation and cortical size through Wee1dependent Cdk1 phosphorylation. J Neurosci. In press.
21. Lin R, Karpa K, Kabbani N, Goldman-Rakic P, Levenson R (2001) Dopamine D2 and D3 receptors are linked to the actin cytoskeleton via interaction with filamin A. Proc Natl Acad Sci U S A 98:5258-5263.
22. Liu G, Thomas L, Warren RA, Enns CA, Cunningham CC, Hartwig JH, Thomas G (1997) Cytoskeletal protein ABP-280 directs the intracellular trafficking of furin and modulates proprotein processing in the endocytic pathway. J Cell Biol 139:1719-1733.
23. Lu J, Sheen V (2005) Periventricular heterotopia. Epilepsy Behav 7:143-149.
24. Lu J, Tiao G, Folkerth R, Hecht J, Walsh C, Sheen V (2006) Overlapping expression of ARFGEF2 and Filamin A in the neuroependymal lining of the lateral ventricles: insights into the cause of periventricular heterotopia. J Comp Neurol 494:476-484.
25. Nadarajah B, Parnavelas JG (2002) Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3:423-432.
26. Nagano T, Morikubo S, Sato M (2004) Filamin A and FILIP (Filamin A-Interacting Protein) regulate cell polarity and motility in neocortical subventricular and intermediate zones during radial migration. J Neurosci 24:9648-9657.
27. Nguyen BP, Gil SG, Carter WG (2000) Deposition of laminin 5 by keratinocytes regulates integrin adhesion and signaling. J Biol Chem 275:31896-31907.
28. O'Connell MP, Fiori JL, Baugher KM, Indig FE, French AD, Camilli TC, Frank BP, Earley R, Hoek KS, Hasskamp JH, Elias EG, Taub DD, Bernier M, Weeraratna AT (2009) Wnt5A activates the calpain-mediated cleavage of filamin A. J Invest Dermatol 129:1782-1789.
29. Ohta Y, Hartwig JH (1995) Actin filament cross-linking by chicken gizzard filamin is regulated by phosphorylation in vitro. Biochemistry 34:6745-6754.
30. Ravid D, Chuderland D, Landsman L, Lavie Y, Reich R, Liscovitch M (2008) Filamin A is a novel caveolin-1-dependent target in IGF-I-stimulated cancer cell migration. Exp Cell Res 314:2762-2773.
31. Robertson SP (2005) Filamin A: phenotypic diversity. Curr Opin Genet Dev 15:301-307.
32. Robertson SP, Twigg SR, Sutherland-Smith AJ, Biancalana V, Gorlin RJ, Horn D, Kenwrick SJ, Kim CA, Morava E, Newbury-Ecob R, Orstavik KH, Quarrell OW, Schwartz CE, Shears DJ, Suri M, Kendrick-Jones J, Wilkie AO; OPD-Spectrum Disorders Clinical Collaborative Group (2003) Localized mutations in the gene encoding the cytoskeletal protein filamin A cause diverse malformations in humans. Nat Genet 33:487-491.
33. Sarkisian MR, Bartley CM, Chi H, Nakamura F, Hashimoto-Torii K, Torii M, Flavell RA, Rakic P (2006) MEKK4 signaling regulates filamin expression and neuronal migration. Neuron 52:789-801.
34. Sheen VL, Feng Y, Graham D, Takafuta T, Shapiro SS, Walsh CA (2002) Filamin A and Filamin B are co-expressed within neurons during periods of neuronal migration and can physically interact. Hum Mol Genet 11:2845-2854.
35. Sheen VL, Ganesh VS, Topcu M, Sebire G, Bodell A, Hill RS, Grant PE, Shugart YY, Imitola J, Khoury SJ, Guerrini R, Walsh CA (2004) Mutations in ARFGEF2 implicate vesicle trafficking in neural progenitor proliferation and migration in the human cerebral cortex. Nat Genet 36:69-76.
36. Shen X, Xu KF, Fan Q, Pacheco-Rodriguez G, Moss J, Vaughan M (2006) Association of brefeldin A-inhibited guanine nucleotide-exchange protein 2 (BIG2) with recycling endosomes during transferrin uptake. Proc Natl Acad Sci U S A 103:2635-2640.
37. Sol é G, Coupry I, Rooryck C, Guérineau E, Martins F, Devés S, Hubert C, Souakri N, Boute O, Marchal C, Faivre L, Landr é E, Debruxelles S, Dieux-Coeslier A, Boulay C, Chassagnon S, Michel V, Routon MC, Toutain A, Philip N, Lacombe D, Villard L, Arveiler B, Goizet C (2009) Bilateral periventricular nodular heterotopia in France: frequency of mutations in FLNA, phenotypic heterogeneity and spectrum of mutations. J Neurol Neurosurg Psychiatry 80:1394-1398.
38. Vadlamudi RK, Li F, Adam L, Nguyen D, Ohta Y, Stossel TP, Kumar R (2002) Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1. Nat Cell Biol 4:681-690.
39. Vicente-Manzanares M, Choi CK, Horwitz AR (2009) Integrins in cell migration-the actin connection. J Cell Sci 122:199-206.
40. Woo MS, Ohta Y, Rabinovitz I, Stossel TP, Blenis J (2004) Ribosomal S6 kinase (RSK) regulates phosphorylation of filamin A on an important regulatory site. Mol Cell Biol 24:3025-3035.
41. Xu W, Baribault H, Adamson ED (1998) Vinculin knockout results in heart and brain defects during embryonic development. Development 125:327-337.
42. Xu Y, Bismar TA, Su J, Xu B, Kristiansen G, Varga Z, Teng L, Ingber DE, Mammoto A, Kumar R, Alaoui-Jamali MA (2010) Filamin A regulates focal adhesion disassembly and suppresses breast cancer cell migration and invasion. J Exp Med 207:2421-2437.
43. Yamaji R, Adamik R, Takeda K, Togawa A, Pacheco-Rodriguez G, Ferrans VJ, Moss J, Vaughan M (2000) Identification and localization of two brefeldin A-inhibited guanine nucleotide-exchange proteins for ADP-ribosylation factors in a macromolecular complex. Proc Natl Acad Sci USA 97:2567-2572.
44. Ziegler WH, Liddington RC, Critchley DR (2006) The structure and regulation of vinculin. Trends Cell Biol 16:453-460.