Table of Contents Author Guidelines Submit a Manuscript
Scientifica
Volume 2012, Article ID 480129, 13 pages
http://dx.doi.org/10.6064/2012/480129
Review Article

Periventricular Heterotopia: Shuttling of Proteins through Vesicles and Actin in Cortical Development and Disease

Department of Neurology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA 02115, USA

Received 2 September 2012; Accepted 14 October 2012

Academic Editors: A. Buettner, G. Pacheco-Rodriguez, and H. Schatten

Copyright © 2012 Volney L. Sheen. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. I. Bystron, C. Blakemore, and P. Rakic, “Development of the human cerebral cortex: boulder Committee revisited,” Nature Reviews Neuroscience, vol. 9, no. 2, pp. 110–122, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Gotz and W. B. Huttner, “The cell biology of neurogenesis,” Nature Reviews Molecular Cell Biology, vol. 6, no. 10, pp. 777–788, 2005. View at Google Scholar
  3. P. Rakic, “Specification of cerebral cortical areas,” Science, vol. 241, no. 4862, pp. 170–176, 1988. View at Google Scholar · View at Scopus
  4. S. Couillard-Despres, J. Winkler, G. Uyanik, and L. Aigner, “Molecular mechanisms of neuronal migration disorders, quo vadis?” Current Molecular Medicine, vol. 1, no. 6, pp. 677–688, 2001. View at Google Scholar · View at Scopus
  5. W. B. Huttner and M. Brand, “Asymmetric division and polarity of neuroepithelial cells,” Current Opinion in Neurobiology, vol. 7, no. 1, pp. 29–39, 1997. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Pontious, T. Kowalczyk, C. Englund, and R. F. Hevner, “Role of intermediate progenitor cells in cerebral cortex development,” Developmental Neuroscience, vol. 30, no. 1–3, pp. 24–32, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. K. I. Mizutani, K. Yoon, L. Dang, A. Tokunaga, and N. Gaiano, “Differential Notch signalling distinguishes neural stem cells from intermediate progenitors,” Nature, vol. 449, no. 7160, pp. 351–355, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Englund, A. Fink, C. Lau et al., “Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex,” Journal of Neuroscience, vol. 25, no. 1, pp. 247–251, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. F. Guillemot, “Cellular and molecular control of neurogenesis in the mammalian telencephalon,” Current Opinion in Cell Biology, vol. 17, no. 6, pp. 639–647, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. A. R. Kriegstein and M. Götz, “Radial glia diversity: a matter of cell fate,” GLIA, vol. 43, no. 1, pp. 37–43, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. J. B. Angevine Jr. and R. L. Sidman, “Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse,” Nature, vol. 192, no. 4804, pp. 766–768, 1961. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Rakic, L. J. Stensas, E. P. Sayre, and R. L. Sidman, “Computer aided three dimensional reconstruction and quantitative analysis of cells from serial electron microscopic montages of foetal monkey brain,” Nature, vol. 250, no. 461, pp. 31–34, 1974. View at Google Scholar · View at Scopus
  13. J. G. Gleeson and C. A. Walsh, “Neuronal migration disorders: from genetic diseases to developmental mechanisms,” Trends in Neurosciences, vol. 23, no. 8, pp. 352–359, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. P. Rakic, “Mode of cell migration to the superficial layers of fetal monkey neocortex,” Journal of Comparative Neurology, vol. 145, no. 1, pp. 61–83, 1972. View at Google Scholar · View at Scopus
  15. N. A. O'Rourke, M. E. Dailey, S. J. Smith, and S. K. McConnell, “Diverse migratory pathways in the developing cerebral cortex,” Science, vol. 258, no. 5080, pp. 299–302, 1992. View at Google Scholar · View at Scopus
  16. C. Walsh and C. L. Cepko, “Widespread dispersion of neuronal clones across functional regions of the cerebral cortex,” Science, vol. 255, no. 5043, pp. 434–440, 1992. View at Google Scholar · View at Scopus
  17. G. Fishell and M. E. Hatten, “Astrotactin provides a receptor system for CNS neuronal migration,” Development, vol. 113, no. 3, pp. 755–765, 1991. View at Google Scholar · View at Scopus
  18. N. A. O'Rourke, A. Chenn, and S. K. McConnell, “Postmitotic neurons migrate tangentially in the cortical ventricular zone,” Development, vol. 124, no. 5, pp. 997–1005, 1997. View at Google Scholar · View at Scopus
  19. J. A. de Carlos, L. López-Mascaraque, and F. Valverde, “Dynamics of cell migration from the lateral ganglionic eminence in the rat,” Journal of Neuroscience, vol. 16, no. 19, pp. 6146–6156, 1996. View at Google Scholar · View at Scopus
  20. S. A. Anderson, D. D. Eisenstat, L. Shi, and J. L. R. Rubenstein, “Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes,” Science, vol. 278, no. 5337, pp. 474–476, 1997. View at Publisher · View at Google Scholar · View at Scopus
  21. A. R. Kriegstein and S. C. Noctor, “Patterns of neuronal migration in the embryonic cortex,” Trends in Neurosciences, vol. 27, no. 7, pp. 392–399, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. A. J. Barkovich, R. Guerrini, R. I. Kuzniecky, G. D. Jackson, W. B. Dobyns et al., “A developmental and genetic classification for malformations of cortical development: update 2012,” Brain, vol. 135, pp. 1348–1369, 2012. View at Google Scholar
  23. G. K. Thornton and C. G. Woods, “Primary microcephaly: do all roads lead to Rome?” Trends in Genetics, vol. 25, no. 11, pp. 501–510, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. P. B. Crino, K. L. Nathanson, and E. P. Henske, “Medical progress: the tuberous sclerosis complex,” The New England Journal of Medicine, vol. 355, no. 13, pp. 1345–1356, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. R. J. Ferland, L. F. Batiz, J. Neal et al., “Disruption of neural progenitors along the ventricular and subventricular zones in periventricular heterotopia,” Human Molecular Genetics, vol. 18, no. 3, pp. 497–516, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. V. L. Sheen, V. S. Ganesh, M. Topcu et al., “Mutations in ARFGEF2 implicate vesicle trafficking in neural progenitor proliferation and migration in the human cerebral cortex,” Nature Genetics, vol. 36, no. 1, pp. 69–76, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. V. L. Sheen, A. Jansen, M. H. Chen et al., “Filamin A mutations cause periventricular heterotopia with Ehlers-Danlos syndrome,” Neurology, vol. 64, no. 2, pp. 254–262, 2005. View at Google Scholar · View at Scopus
  28. J. W. Fox, E. D. Lamperti, Y. Z. Ekşioǧlu et al., “Mutations in filamin 1 prevent migration of cerebral cortical neurons in human Periventricular heterotopia,” Neuron, vol. 21, no. 6, pp. 1315–1325, 1998. View at Publisher · View at Google Scholar · View at Scopus
  29. M. C. de Wit, I. F. de Coo, D. J. Halley, M. H. Lequin, and G. M. Mancini, “Movement disorder and neuronal migration disorder due to ARFGEF2 mutation,” Neurogenetics, vol. 10, no. 4, pp. 333–336, 2009. View at Google Scholar · View at Scopus
  30. K. Poirier, D. A. Keays, F. Francis et al., “Large spectrum of lissencephaly and pachygyria phenotypes resulting from de novo missense mutations in tubulin alpha 1A (TUBA1A),” Human Mutation, vol. 28, no. 11, pp. 1055–1064, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. M. R. Abdollahi, E. Morrison, T. Sirey et al., “Mutation of the Variant α-Tubulin TUBA8 Results in Polymicrogyria with Optic Nerve Hypoplasia,” American Journal of Human Genetics, vol. 85, no. 5, pp. 737–744, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. X. H. Jaglin and J. Chelly, “Tubulin-related cortical dysgeneses: microtubule dysfunction underlying neuronal migration defects,” Trends in Genetics, vol. 25, no. 12, pp. 555–566, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Lu and V. Sheen, “Periventricular heterotopia,” Epilepsy and Behavior, vol. 7, no. 2, pp. 143–149, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. V. L. Sheen, M. Topçu, S. Berkovic et al., “Autosomal recessive form of periventricular heterotopia,” Neurology, vol. 60, no. 7, pp. 1108–1112, 2003. View at Google Scholar · View at Scopus
  35. Y. Feng and C. A. Walsh, “The many faces of filamin: a versatile molecular scaffold for cell motility and signalling,” Nature Cell Biology, vol. 6, no. 11, pp. 1034–1038, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. V. L. Sheen, J. W. Wheless, A. Bodell et al., “Periventricular heterotopia associated with chromosome 5p anomalies,” Neurology, vol. 60, no. 6, pp. 1033–1036, 2003. View at Google Scholar · View at Scopus
  37. R. J. Ferland, J. N. Gaitanis, K. Apse, U. Tantravahi, C. A. Walsh, and V. L. Sheen, “Periventricular nodular heterotopia and Williams syndrome,” American Journal of Medical Genetics A, vol. 140, no. 12, pp. 1305–1311, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Cellini, V. Disciglio, F. Novara et al., “Periventricular heterotopia with white matter abnormalities associated with 6p25 deletion,” American Journal of Medical Genetics A, vol. 158, no. 7, pp. 1793–1797, 2012. View at Google Scholar
  39. M. B. Ramocki, M. Bartnik, P. Szafranski et al., “Recurrent distal 7q11.23 deletion including HIP1 and YWHAG identified in patients with intellectual disabilities, epilepsy, and neurobehavioral problems,” American Journal of Human Genetics, vol. 87, no. 6, pp. 857–865, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Neal, K. Apse, M. Sahin, C. A. Walsh, and V. L. Sheen, “Deletion of chromosome 1p36 is associated with periventricular nodular heterotopia,” American Journal of Medical Genetics A, vol. 140, no. 15, pp. 1692–1695, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Gawlik-Kuklinska, J. Wierzba, A. Wozniak et al., “Periventricular heterotopia in a boy with interstitial deletion of chromosome 4p,” European Journal of Medical Genetics, vol. 51, no. 2, pp. 165–171, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. R. Guerrini, C. Cardoso, A. Boys et al., “Periventricular heterotopia, mental retardation, and epilepsy associated with 5q14.3–q15 deletion,” Neurology, vol. 72, no. 9, pp. 784–792, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. F. Moro, T. Pisano, B. D. Bernardina et al., “Periventricular heterotopia in fragile X syndrome,” Neurology, vol. 67, no. 4, pp. 713–715, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. V. L. Sheen, A. R. Torres, X. Du, B. Barry, C. A. Walsh, and V. E. Kimonis, “Mutation in PQBP1 is associated with periventricular heterotopia,” American Journal of Medical Genetics A, vol. 152, no. 11, pp. 2888–2890, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Truant, R. Atwal, and A. Burtnik, “Hypothesis: huntingtin may function in membrane association and vesicular trafficking,” Biochemistry and Cell Biology, vol. 84, no. 6, pp. 912–917, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. H. Soumiya, H. Fukumitsu, and S. Furukawa, “Stem cell factor induces heterotopic accumulation of cells (heterotopia) in the mouse cerebral cortex,” Biomedical Research, vol. 30, no. 2, pp. 121–128, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Cappello, A. Attardo, X. Wu et al., “The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface,” Nature Neuroscience, vol. 9, no. 9, pp. 1099–1107, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. T. N. Phoenix and S. Temple, “Spred1, a negative regulator of Ras-MAPK-ERK, is enriched in CNS germinal zones, dampens NSC proliferation, and maintains ventricular zone structure,” Genes and Development, vol. 24, no. 1, pp. 45–56, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. M. R. Sarkisian, C. M. Bartley, H. Chi et al., “MEKK4 Signaling regulates Filamin expression and neuronal migration,” Neuron, vol. 52, no. 5, pp. 789–801, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. D. O. Clary, I. C. Griff, and J. E. Rothman, “SNAPs, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast,” Cell, vol. 61, no. 4, pp. 709–721, 1990. View at Publisher · View at Google Scholar · View at Scopus
  51. V. L. Sheen, P. H. Dixon, J. W. Fox et al., “Mutations in the X-linked filamin 1 gene cause periventricular nodular heterotopia in males as well as in females,” Human Molecular Genetics, vol. 10, no. 17, pp. 1775–1783, 2001. View at Google Scholar · View at Scopus
  52. E. Reinstein, B. S. Chang, S. P. Robertson et al., “Filamin A mutation associated with normal reading skills and dyslexia in a family with periventricular heterotopia,” American Journal of Medical Genetics A, vol. 158, no. 8, pp. 1897–18901.
  53. M. V. Felker, L. M. Walker, D. K. Sokol et al., “Early cognitive and behavioral problems in children with nodular heterotopia,” Epilepsy & Behavior, vol. 22, no. 3, pp. 523–526, 2011. View at Google Scholar
  54. R. Guerrini, D. Mei, S. Sisodiya et al., “Germline and mosaic mutations of FLN1 in men with periventricular heterotopia,” Neurology, vol. 63, no. 1, pp. 51–56, 2004. View at Google Scholar · View at Scopus
  55. M. Gérard-Blanluet, V. Sheen, K. Machinis et al., “Bilateral periventricular heterotopias in an X-linked dominant transmission in a family with two affected males,” American Journal of Medical Genetics, vol. 140, no. 10, pp. 1041–1046, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. G. Solé, I. Coupry, C. Rooryck et al., “Bilateral periventricular nodular heterotopia in France: frequency of mutations in FLNA, phenotypic heterogeneity and spectrum of mutations,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 80, no. 12, pp. 1394–1398, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. E. Parrini, A. Ramazzotti, W. B. Dobyns et al., “Periventricular heterotopia: phenotypic heterogeneity and correlation with Filamin a mutations,” Brain, vol. 129, no. 7, pp. 1892–1906, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. A. R. Clark, G. M. Sawyer, S. P. Robertson, and A. J. Sutherland-Smith, “Skeletal dysplasias due to filamin A mutations result from a gain-of-function mechanism distinct from allelic neurological disorders,” Human Molecular Genetics, vol. 18, no. 24, pp. 4791–4800, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. S. P. Robertson, S. R. Twigg, A. J. Sutherland-Smith et al., “Localized mutations in the gene encoding the cytoskeletal protein filamin A cause diverse malformations in humans,” Nature Genetics, vol. 33, no. 4, pp. 487–491, 2003. View at Google Scholar
  60. E. Parrini, I. L. Rivas, J. F. Toral et al., “In-frame deletion in FLNA causing familial periventricular heterotopia with skeletal dysplasia in males,” American Journal of Medical Genetics A, vol. 155, no. 5, pp. 1140–1146, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. Y. Sun, R. Almomani, E. Aten et al., “Terminal osseous dysplasia is caused by a single recurrent mutation in the FLNA gene,” American Journal of Human Genetics, vol. 87, no. 1, pp. 146–153, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. P. Gómez-Garre, M. Seijo, E. Gutiérrez-Delicado et al., “Ehlers-Danlos syndrome and periventricular nodular heterotopia in a Spanish family with a single FLNA mutation,” Journal of Medical Genetics, vol. 43, no. 3, pp. 232–237, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. M. C. de Wit, I. F. M. de Coo, M. H. Lequin et al., “Combined cardiological and neurological abnormalities due to filamin A gene mutation,” Clinical Research in Cardiology, vol. 100, no. 1, pp. 45–50.
  64. F. Kyndt, J. P. Gueffet, V. Probst et al., “Mutations in the gene encoding filamin A as a cause for familial cardiac valvular dystrophy,” Circulation, vol. 115, no. 1, pp. 40–49, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. M. C. Y. de Wit, H. A. W. M. Tiddens, I. F. M. de Coo, and G. M. S. Mancini, “Lung disease in FLNA mutation: confirmatory report,” European Journal of Medical Genetics, vol. 54, no. 3, pp. 299–300, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Masurel-Paulet, E. Haan, E. M. Thompson et al., “Lung disease associated with periventricular nodular heterotopia and an FLNA mutation,” European Journal of Medical Genetics, vol. 54, no. 1, pp. 25–28, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Gargiulo, R. Auricchio, M. V. Barone et al., “Filamin A is mutated in X-linked chronic idiopathic intestinal pseudo-obstruction with central nervous system involvement,” American Journal of Human Genetics, vol. 80, no. 4, pp. 751–758, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. R. P. Kapur, S. P. Robertson, M. C. Hannibal et al., “Diffuse abnormal layering of small intestinal smooth muscle is present in patients with FLNA mutations and X-linked intestinal pseudo-obstruction,” American Journal of Surgical Pathology, vol. 34, no. 10, pp. 1528–1543, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. J. Clayton-Smith, S. Walters, E. Hobson et al., “Xq28 duplication presenting with intestinal and bladder dysfunction and a distinctive facial appearance,” European Journal of Human Genetics, vol. 17, no. 4, pp. 434–443, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. C. Chakarova, M. S. Wehnert, K. Uhl et al., “Genomic structure and fine mapping of the two human filamin gene paralogues FLNB and FLNC and comparative analysis of the filamin gene family,” Human Genetics, vol. 107, no. 6, pp. 597–611, 2000. View at Publisher · View at Google Scholar · View at Scopus
  71. V. L. Sheen, Y. Feng, D. Graham, T. Takafuta, S. S. Shapiro, and C. A. Walsh, “Filamin A and Filamin B are co-expressed within neurons during periods of neuronal migration and can physically interact,” Human Molecular Genetics, vol. 11, no. 23, pp. 2845–2854, 2002. View at Google Scholar · View at Scopus
  72. J. B. Gorlin, R. Yamin, S. Egan et al., “Human endothelial actin-binding protein (ABP-280, nonmuscle filamin): a molecular leaf spring,” Journal of Cell Biology, vol. 111, no. 3, pp. 1089–1105, 1990. View at Publisher · View at Google Scholar · View at Scopus
  73. C. C. Cunningham, J. B. Gorlin, D. J. Kwiatkowski et al., “Actin-binding protein requirement for cortical stability and efficient locomotion,” Science, vol. 255, no. 5042, pp. 325–327, 1992. View at Google Scholar · View at Scopus
  74. J. H. Hartwig and P. Shevlin, “The architecture of actin filaments and the ultrastructural location of actin-binding protein in the periphery of lung macrophages,” Journal of Cell Biology, vol. 103, no. 3, pp. 1007–1020, 1986. View at Google Scholar · View at Scopus
  75. J. H. Hartwig, J. Tyler, and T. P. Stossel, “Actin-binding protein promotes the bipolar and perpendicular branching of actin filaments,” Journal of Cell Biology, vol. 87, no. 3, pp. 841–848, 1980. View at Google Scholar · View at Scopus
  76. R. K. Vadlamudi, F. Li, L. Adam et al., “Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1,” Nature Cell Biology, vol. 4, no. 9, pp. 681–690, 2002. View at Publisher · View at Google Scholar · View at Scopus
  77. J. M. Dyson, C. J. O'Malley, J. Becanovic et al., “The SH2-containing inositol polyphosphate 5-phosphatase, SHIP-2, binds filamin and regulates submembraneous actin,” Journal of Cell Biology, vol. 155, no. 6, pp. 1065–1079, 2001. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Marti, Z. Luo, C. Cunningham et al., “Actin-biding protein-280 binds the stress-activated protein kinase (SAPK) activator SEK-1 and is required for tumor necrosis factor-α activation of SAPK in melanoma cells,” Journal of Biological Chemistry, vol. 272, no. 5, pp. 2620–2628, 1997. View at Publisher · View at Google Scholar · View at Scopus
  79. M. S. Woo, Y. Ohta, I. Rabinovitz, T. P. Stossel, and J. Blenis, “Ribosomal S6 Kinase (RSK) regulates phosphorylation of filamin a on an important regulatory site,” Molecular and Cellular Biology, vol. 24, no. 7, pp. 3025–3035, 2004. View at Publisher · View at Google Scholar · View at Scopus
  80. Z. Razinia, T. Mäkelä, J. Ylänne et al., “Filamins in mechanosensing and signaling,” Annual Review of Biophysics, vol. 41, pp. 227–246, 2012. View at Google Scholar
  81. D. T. Loo, S. B. Kanner, and A. Aruffo, “Filamin binds to the cytoplasmic domain of the β1-integrin: identification of amino acids responsible for this interaction,” Journal of Biological Chemistry, vol. 273, no. 36, pp. 23304–23312, 1998. View at Publisher · View at Google Scholar · View at Scopus
  82. E. Peverelli, G. Mantovani, E. Vitali et al., “Filamin-A is essential for dopamine d2 receptor expression and signaling in tumorous lactotrophs,” Journal of Clinical Endocrinology & Metabolism, vol. 97, no. 3, pp. 967–977.
  83. J. L. Fiori, T. N. Zhu, M. P. O'Connell et al., “Filamin a modulates kinase activation and intracellular trafficking of epidermal growth factor receptors in human melanoma cells,” Endocrinology, vol. 150, no. 6, pp. 2551–2560, 2009. View at Publisher · View at Google Scholar · View at Scopus
  84. D. M. Ozanne, M. E. Brady, S. Cook, L. Gaughan, D. E. Neal, and C. N. Robson, “Androgen receptor nuclear translocation is facilitated by the f-actin cross-linking protein filamin,” Molecular Endocrinology, vol. 14, no. 10, pp. 1618–1626, 2000. View at Google Scholar · View at Scopus
  85. C. J. Loy, K. S. Sim, and E. L. Yong, “Filamin-A fragment localizes to the nucleus to regulate androgen receptor and coactivator functions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 8, pp. 4562–4567, 2003. View at Publisher · View at Google Scholar · View at Scopus
  86. W. R. Thelin, Y. Chen, M. Gentzsch et al., “Direct interaction with filamins modulates the stability and plasma membrane expression of CFTR,” Journal of Clinical Investigation, vol. 117, no. 2, pp. 364–374, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. T. Seck, R. Baron, and W. C. Horne, “Binding of filamin to the C-terminal tail of the calcitonin receptor controls recycling,” Journal of Biological Chemistry, vol. 278, no. 12, pp. 10408–10416, 2003. View at Publisher · View at Google Scholar · View at Scopus
  88. J. M. Beekman, C. E. Van Der Poel, J. A. Van Der Linden et al., “Filamin A stabilizes FcγRI surface expression and prevents its lysosomal routing,” Journal of Immunology, vol. 180, no. 6, pp. 3938–3945, 2008. View at Google Scholar · View at Scopus
  89. S. Jiménez-Baranda, C. Gómez-Moutón, A. Rojas et al., “Filamin-A regulates actin-dependent clustering of HIV receptors,” Nature Cell Biology, vol. 9, no. 7, pp. 838–846, 2007. View at Publisher · View at Google Scholar · View at Scopus
  90. R. Leung, Y. Wang, K. Cuddy et al., “Filamin A regulates monocyte migration through rho small GTPases during osteoclastogenesis,” Journal of Bone and Mineral Research, vol. 25, no. 5, pp. 1077–1091, 2010. View at Publisher · View at Google Scholar · View at Scopus
  91. Y. Ohta, J. H. Hartwig, and T. P. Stossel, “FilGAP, a Rho- and ROCK-regulated GAP for Rac binds filamin A to control actin remodelling,” Nature Cell Biology, vol. 8, no. 8, pp. 803–814, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. Z. Yang, S. Rayala, D. Nguyen, R. K. Vadlamudi, S. Chen, and R. Kumar, “Pak1 phosphorylation of Snail, a master regulator of epithelial-to- mesenchyme transition, modulates Snail's subcellular localization and functions,” Cancer Research, vol. 65, no. 8, pp. 3179–3184, 2005. View at Google Scholar · View at Scopus
  93. P. Grimbert, A. Valanciute, V. Audard, P. Lang, G. Guellaën, and D. Sahali, “The Filamin-A is a partner of Tc-mip, a new adapter protein involved in c-maf-dependent Th2 signaling pathway,” Molecular Immunology, vol. 40, no. 17, pp. 1257–1261, 2004. View at Publisher · View at Google Scholar · View at Scopus
  94. H. Teramoto, O. A. Coso, H. Miyata, T. Igishi, T. Miki, and J. Silvio Gutkind, “Signaling from the small GTP-binding proteins Rac1 and Cdc42 to the c- Jun N-terminal kinase/stress-activated protein kinase pathway: a role for mixed lineage kinase 3/protein-tyrosine kinase 1, a novel member of the mixed lineage kinase family,” Journal of Biological Chemistry, vol. 271, no. 44, pp. 27225–27228, 1996. View at Publisher · View at Google Scholar · View at Scopus
  95. H. Kim and C. A. McCulloch, “Filamin A mediates interactions between cytoskeletal proteins that control cell adhesion,” FEBS Letters, vol. 585, no. 1, pp. 18–22, 2011. View at Publisher · View at Google Scholar · View at Scopus
  96. A. J. Ehrlicher, F. Nakamura, J. H. Hartwig et al., “Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A,” Nature, vol. 478, no. 7368, pp. 260–263.
  97. A. W. Hart, J. E. Morgan, J. Schneider et al., “Cardiac malformations and midline skeletal defects in mice lacking filamin A,” Human Molecular Genetics, vol. 15, no. 16, pp. 2457–2467, 2006. View at Publisher · View at Google Scholar · View at Scopus
  98. Y. Feng, M. H. Chen, I. P. Moskowitz et al., “Filamin a (FLNA) is required for cell-cell contact in vascular development and cardiac morphogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 52, pp. 19836–19841, 2006. View at Publisher · View at Google Scholar · View at Scopus
  99. G. Lian, J. Lu, J. Hu et al., “Filamin a regulates neural progenitor proliferation and cortical size through Wee1-dependent Cdk1 phosphorylation,” Journal of Neuroscience, vol. 32, no. 22, pp. 7672–7684, 2012. View at Google Scholar
  100. M. H. Nunnally, J. M. D'Angelo, and S. W. Craig, “Filamin concentration in cleavage furrow and midbody region: frequency of occurrence compared with that of alpha-actinin and myosin,” Journal of Cell Biology, vol. 87, no. 1, pp. 219–226, 1980. View at Google Scholar · View at Scopus
  101. T. Nagano, S. Morikubo, and M. Sato, “Filamin A and FILIP (Filamin A-interacting protein) regulate cell polarity and motility in neocortical subventricular and intermediate zones during radial migration,” Journal of Neuroscience, vol. 24, no. 43, pp. 9648–9657, 2004. View at Publisher · View at Google Scholar · View at Scopus
  102. T. Nagano, T. Yoneda, Y. Hatanaka, C. Kubota, F. Murakami, and M. Sato, “Filamin A-interacting protein (FILIP) regulates cortical cell migration out of the ventricular zone,” Nature Cell Biology, vol. 4, no. 7, pp. 495–501, 2002. View at Publisher · View at Google Scholar · View at Scopus
  103. J. Zhang, J. Neal, G. Lian et al., “Brefeldin A-inhibited guanine exchange factor 2 regulates Filamin A phosphorylation and neuronal migration,” Journal of Neuroscience, vol. 32, no. 36, pp. 12619–12629, 2012. View at Google Scholar
  104. H. W. Shin, N. Morinaga, M. Noda, and K. Nakayama, “BIG2, A guanine nucleotide exchange factor for ADP-ribosylation factors: its localization to recycling endosomes and implication in the endosome integrity,” Molecular Biology of the Cell, vol. 15, no. 12, pp. 5283–5294, 2004. View at Publisher · View at Google Scholar · View at Scopus
  105. T. Achstetter, A. Franzusoff, C. Field, and R. Schekman, “SEC7 encodes an unusual, high molecular weight protein required for membrane traffic from the yeast Golgi apparatus,” Journal of Biological Chemistry, vol. 263, no. 24, pp. 11711–11717, 1988. View at Google Scholar · View at Scopus
  106. M. Sata, J. G. Donaldson, J. Moss, and M. Vaughan, “Brefeldin A-inhibited guanine nucleotide-exchange activity of Sec7 domain from yeast Sec7 with yeast and mammalian ADP ribosylation factors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 8, pp. 4204–4208, 1998. View at Publisher · View at Google Scholar · View at Scopus
  107. A. Togawa, N. Morinaga, M. Ogasawara, J. Moss, and M. Vaughan, “Purification and cloning of a brefeldin A-inhibited guanine nucleotide- exchange protein for ADP-ribosylation factors,” Journal of Biological Chemistry, vol. 274, no. 18, pp. 12308–12315, 1999. View at Publisher · View at Google Scholar · View at Scopus
  108. G. Pacheco-Rodriguez, J. Moss, and M. Vaughan, “BIG1 and BIG2: brefeldin A-inhibited guanine nucleotide-exchange proteins for ADP-ribosylation factors,” Methods in Enzymology, vol. 345, pp. 397–404, 2001. View at Publisher · View at Google Scholar · View at Scopus
  109. H. D. Jones, J. Moss, and M. Vaughan, “BIG1 and BIG2, brefeldin A-inhibited guanine nucleotide-exchange factors for ADP-ribosylation factors,” Methods in Enzymology, vol. 404, pp. 174–184, 2005. View at Publisher · View at Google Scholar · View at Scopus
  110. C. Shinotsuka, S. Waguri, M. Wakasugi, Y. Uchiyama, and K. Nakayama, “Dominant-negative mutant of BIG2, an ARF-guanine nucleotide exchange factor, specifically affects membrane trafficking from the trans-Golgi network through inhibiting membrane association of AP-1 and GGA coat proteins,” Biochemical and Biophysical Research Communications, vol. 294, no. 2, pp. 254–260, 2002. View at Publisher · View at Google Scholar · View at Scopus
  111. C. Shinotsuka, Y. Yoshida, K. Kawamoto, H. Takatsu, and K. Nakayama, “Overexpression of an ADP-ribosylation factor-guanine nucleotide exchange factor, BIG2, uncouples brefeldin A-induced adaptor protein-1 coat dissociation and membrane tubulation,” Journal of Biological Chemistry, vol. 277, no. 11, pp. 9468–9473, 2002. View at Publisher · View at Google Scholar · View at Scopus
  112. H. W. Shin, C. Shinotsuka, and K. Nakayama, “Expression of BIG2 and analysis of its function in mammalian cells,” Methods in Enzymology, vol. 404, pp. 206–215, 2005. View at Publisher · View at Google Scholar · View at Scopus
  113. H. Li, R. Adamik, G. Pacheco-Rodriguez, J. Moss, and M. Vaughan, “Protein kinase A-anchoring (AKAP) domains in brefeldin A-inhibited guanine nucleotide-exchange protein 2 (BIG2),” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 4, pp. 1627–1632, 2003. View at Publisher · View at Google Scholar · View at Scopus
  114. E. I. Charych, W. Yu, C. P. Miralles et al., “The brefeldin A-inhibited GDP/GTP exchange factor 2, a protein involved in vesicular trafficking, interacts with the β subunits of the GABA A receptors,” Journal of Neurochemistry, vol. 90, no. 1, pp. 173–189, 2004. View at Publisher · View at Google Scholar · View at Scopus
  115. W. Wong and J. D. Scott, “AKAP signalling complexes: focal points in space and time,” Nature Reviews Molecular Cell Biology, vol. 5, no. 12, pp. 959–970, 2004. View at Publisher · View at Google Scholar · View at Scopus
  116. F. Kuroda, J. Moss, and M. Vaughan, “Regulation of brefeldin A-inhibited guanine nucleotide-exchange protein 1 (BIG1) and BIG2 activity via PKA and protein phosphatse 1γ,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 9, pp. 3201–3206, 2007. View at Publisher · View at Google Scholar · View at Scopus
  117. C. D'Souza-Schorey and P. Chavrier, “ARF proteins: roles in membrane traffic and beyond,” Nature Reviews Molecular Cell Biology, vol. 7, no. 5, pp. 347–358, 2006. View at Publisher · View at Google Scholar · View at Scopus
  118. C. J. Zhang, A. G. Rosenwald, M. C. Willingham, S. Skuntz, J. Clark, and R. A. Kahn, “Expression of a dominant allele of human ARF1 inhibits membrane traffic in vivo,” Journal of Cell Biology, vol. 124, no. 3, pp. 289–300, 1994. View at Google Scholar · View at Scopus
  119. J. M. Lenhard, R. A. Kahn, and P. D. Stahl, “Evidence for ADP-ribosylation factor (ARF) as a regulator of in vitro endosome-endosome fusion,” Journal of Biological Chemistry, vol. 267, no. 18, pp. 13047–13052, 1992. View at Google Scholar · View at Scopus
  120. J. Lu, G. Tiao, R. Folkerth, J. Hecht, C. Walsh, and V. Sheen, “Overlapping expression of ARFGEF2 and filamin A in the neuroependymal lining of the lateral ventricles: insights into the cause of periventricular heterotopia,” Journal of Comparative Neurology, vol. 494, no. 3, pp. 476–484, 2006. View at Publisher · View at Google Scholar · View at Scopus
  121. P. Grzmil, Z. Enkhbaatar, B. Gundsambuu et al., “Early embryonic lethality in gene trap mice with disruption of the Arfgef2 gene,” International Journal of Developmental Biology, vol. 54, no. 8-9, pp. 1259–1266, 2010. View at Publisher · View at Google Scholar · View at Scopus
  122. J. J. Jung, S. M. Inamdar, and A. Choudhury, “Regulation of intracellular membrane trafficking and cell dynamics by syntaxin-6,” Bioscience Reports, vol. 32, no. 4, pp. 383–391, 2012. View at Google Scholar
  123. A. D. Gillon, C. F. Latham, and E. A. Miller, “Vesicle-mediated ER export of proteins and lipids,” Biochimica et Biophysica Acta, no. 8, pp. 1040–1049, 1821. View at Google Scholar
  124. V. Cavalli, M. Corti, and J. Gruenberg, “Endocytosis and signaling cascades: a close encounter,” FEBS Letters, vol. 498, no. 2-3, pp. 190–196, 2001. View at Publisher · View at Google Scholar · View at Scopus
  125. R. L. Jeng and M. D. Welch, “Cytoskeleton actin and endocytosis—no longer the weakest link,” Current Biology, vol. 11, no. 17, pp. R691–R694, 2001. View at Publisher · View at Google Scholar · View at Scopus
  126. G. Liu, L. Thomas, R. A. Warren et al., “Cytoskeletal protein ABP-280 directs the intracellular trafficking of furin and modulates proprotein processing in the endocytic pathway,” Journal of Cell Biology, vol. 139, no. 7, pp. 1719–1733, 1997. View at Publisher · View at Google Scholar · View at Scopus
  127. M. Sverdlov, V. Shinin, A. T. Place, M. Castellon, and R. D. Minshall, “Filamin A regulates caveolae internalization and trafficking in endothelial cells,” Molecular Biology of the Cell, vol. 20, no. 21, pp. 4531–4540, 2009. View at Publisher · View at Google Scholar · View at Scopus
  128. A. V. Andreeva, M. A. Kutuzov, R. Vaiskunaite et al., “G alpha12 interaction with alphaSNAP induces VE-cadherin localization at endothelial junctions and regulates barrier function,” Journal of Biological Chemistry, vol. 280, no. 34, pp. 30376–30383, 2005. View at Google Scholar
  129. L. Rönnstrand, “Signal transduction via the stem cell factor receptor/c-Kit,” Cellular and Molecular Life Sciences, vol. 61, no. 19-20, pp. 2535–2548, 2004. View at Publisher · View at Google Scholar · View at Scopus