Skip to main content

Actin Cytoskeletal Regulation in Neuronal Migration

  • Chapter
  • First Online:
Neurobiology of Actin

Part of the book series: Advances in Neurobiology ((NEUROBIOL,volume 5))

  • 785 Accesses

Abstract

Polymerization of actin has many functions in motile cells, ranging from assisting with subcellular localization of proteins important to polarization, generation of motive forces, cell adhesion, alteration of membrane shape, and even intracellular protein trafficking. While the broad strokes of these events are similar among cell types, recent studies indicate significant differences for neuronal motility compared with epithelial and fibroblast cells. This chapter discusses current insights into the role and regulation of F-actin dynamics in the steps required for neuronal migration.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alberti S, Krause SM, Kretz O, Philippar U, Lemberger T, Casanova E, Wiebel FF, Schwarz H, Frotscher M, Schütz G, Nordheim A (2005) Neuronal migration in the murine rostral migratory stream requires serum response factor. Proc Natl Acad Sci U S A 102:6148–53.

    Article  PubMed  CAS  Google Scholar 

  • Angata K, Huckaby V, Ranscht B, Terskikh A, Marth JD, Fukuda M (2007) Polysialic acid-directed migration and differentiation of neural precursors are essential for mouse brain development. Mol Cell Biol 27:6659–6668.

    Article  PubMed  CAS  Google Scholar 

  • Anton ES, Kreidberg JA, Rakic P (1999) Distinct functions of alpha3 and alpha(v) integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron 22:277–289.

    Article  PubMed  CAS  Google Scholar 

  • Arregui CO, Carbonetto S, McKerracher L (1994) Characterization of neural cell adhesion sites: point contacts are the sites of interaction between integrins and the cytoskeleton in PC12 cells. J Neurosci 14:6967–6977.

    PubMed  CAS  Google Scholar 

  • Balenci L, Saoudi Y, Grunwald D, Deloulme JC, Bouron A, Bernards A, Baudier J (2007) IQGAP1 regulates adult neural progenitors in vivo and vascular endothelial growth factor-triggered neural progenitor migration in vitro. J Neurosci 27:4716–4724.

    Article  PubMed  CAS  Google Scholar 

  • Bar I, Lambert de Rouvroit C, Goffinet AM (2000) The Reelin signaling pathway in mouse cortical development. Eur J Morphol 38:321–325.

    Article  PubMed  CAS  Google Scholar 

  • Bear JE, Svitkina TM, Krause M, Schafer DA, Loureiro JJ, Strasser GA, Maly IV, Chaga OY, Cooper JA, Borisy GG, Gertler FB (2002) Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109:509–521.

    Article  PubMed  CAS  Google Scholar 

  • Beggs HE, Baragona SC, Hemperly JJ, Maness PF (1997) NCAM140 interacts with the focal adhesion kinase p125(fak) and the SRC-related tyrosine kinase p59(fyn). J Biol Chem 272:8310–8319.

    Article  PubMed  CAS  Google Scholar 

  • Bellenchi GC, Gurniak CB, Perlas E, Middei S, Ammassari-Teule M, Witke W (2007) N-cofilin is associated with neuronal migration disorders and cell cycle control in the cerebral cortex. Genes Dev 21:2347–2357.

    Article  PubMed  CAS  Google Scholar 

  • Benachenhou N, Massy I, Vacher J (2002) Characterization and expression analyses of the mouse Wiskott–Aldrich syndrome protein (WASP) family member Wave1/Scar. Gene 290:131–140.

    Article  PubMed  CAS  Google Scholar 

  • Bensenor LB, Kan HM, Wang N, Wallrabe H, Davidson LA, Cai Y, Schafer DA, Bloom GS (2007) IQGAP1 regulates cell motility by linking growth factor signaling to actin assembly. J Cell Sci 120:658–669.

    Article  PubMed  CAS  Google Scholar 

  • Billuart P, Bienvenu T, Ronce N, des Portes V, Vinet MC, Zemni R, Roest Crollius H, Carrie A, Fauchereau F, Cherry M, Briault S, Hamel B, Fryns JP, Beldjord C, Kahn A, Moraine C, Chelly J (1998) Oligophrenin-1 encodes a rhoGAP protein involved in X-linked mental retardation. Nature 392:923–926.

    Google Scholar 

  • Bishop AL, Hall A (2000) Rho GTPases and their effector proteins. Biochem J 348(Pt 2):241–255.

    Article  PubMed  CAS  Google Scholar 

  • Bock HH, Herz J (2003) Reelin activates SRC family tyrosine kinases in neurons. Curr Biol 13:18–26.

    Article  PubMed  CAS  Google Scholar 

  • Bodrikov V, Leshchyns’ka I, Sytnyk V, Overvoorde J, den Hertog J, Schachner M (2005) RPTPalpha is essential for NCAM-mediated p59fyn activation and neurite elongation. J Cell Biol 168:127–139.

    Article  PubMed  CAS  Google Scholar 

  • Boycott KM, Flavelle S, Bureau A, Glass HC, Fujiwara TM, Wirrell E, Davey K, Chudley AE, Scott JN, McLeod DR, Parboosingh JS (2005) Homozygous deletion of the very low density lipoprotein receptor gene causes autosomal recessive cerebellar hypoplasia with cerebral gyral simplification. Am J Hum Genet 77:477–483.

    Article  PubMed  CAS  Google Scholar 

  • Brown MD, Sacks DB (2006) IQGAP1 in cellular signaling: bridging the GAP. Trends Cell Biol 16:242–249.

    Article  PubMed  CAS  Google Scholar 

  • Castets M, Schaeffer C, Bechara E, Schenck A, Khandjian EW, Luche S, Moine H, Rabilloud T, Mandel JL, Bardoni B (2005) FMRP interferes with the Rac1 pathway and controls actin cytoskeleton dynamics in murine fibroblasts. Hum Mol Genet 14:835–844.

    Article  PubMed  CAS  Google Scholar 

  • Cooper JA, Pollard TD (1985) Effect of capping protein on the kinetics of actin polymerization. Biochemistry 24:793–799.

    Article  PubMed  CAS  Google Scholar 

  • Cooper JA, Schafer DA (2000) Control of actin assembly and disassembly at filament ends. Curr Opin Cell Biol 12:97–103.

    Article  PubMed  CAS  Google Scholar 

  • Dahl JP, Wang-Dunlop J, Gonzales C, Goad ME, Mark RJ, Kwak SP (2003) Characterization of the WAVE1 knock-out mouse: implications for CNS development. J Neurosci 23:3343–3352.

    PubMed  CAS  Google Scholar 

  • Dequidt C, Danglot L, Alberts P, Galli T, Choquet D, Thoumine O (2007) Fast turnover of L1 adhesions in neuronal growth cones involving both surface diffusion and exo/endocytosis of L1 molecules. Mol Biol Cell 18:3131–3143.

    Article  PubMed  CAS  Google Scholar 

  • des Portes V, Boddaert N, Sacco S, Briault S, Maincent K, Bahi N, Gomot M, Ronce N, Bursztyn J, Adamsbaum C, Zilbovicius M, Chelly J, Moraine C (2004) Specific clinical and brain MRI features in mentally retarded patients with mutations in the oligophrenin-1 gene. Am J Med Genet A 124:364–371.

    Article  Google Scholar 

  • Dulabon L, Olson EC, Taglienti MG, Eisenhuth S, McGrath B, Walsh CA, Kreidberg JA, Anton ES (2000) Reelin binds alpha3beta1 integrin and inhibits neuronal migration. Neuron 27:33–44.

    Article  PubMed  CAS  Google Scholar 

  • D’Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler [see comments]. Nature 374:719–723.

    Article  PubMed  Google Scholar 

  • Edmondson JC, Hatten ME (1987) Glial-guided granule neuron migration in vitro: a high-resolution time-lapse video microscopic study. J Neurosci 7:1928–1934.

    PubMed  CAS  Google Scholar 

  • Etienne-Manneville S, Manneville JB, Nicholls S, Ferenczi MA, Hall A (2005) Cdc42 and Par6-PKCzeta regulate the spatially localized association of Dlg1 and APC to control cell polarization. J Cell Biol 170:895–901.

    Article  PubMed  CAS  Google Scholar 

  • Faix J, Grosse R (2006) Staying in shape with formins. Dev Cell 10:693–706.

    Article  PubMed  CAS  Google Scholar 

  • Fox JW, Lamperti ED, Eksioglu YZ, Hong SE, Feng Y, Graham DA, Scheffer IE, Dobyns WB, Hirsch BA, Radtke RA, Berkovic SF, Huttenlocher PR, Walsh CA (1998) Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia. Neuron 21:1315–1325.

    Article  PubMed  CAS  Google Scholar 

  • Fukuoka M, Miki H, Takenawa T (1997) Identification of N-WASP homologs in human and rat brain. Gene 196:43–48.

    Article  PubMed  CAS  Google Scholar 

  • Garvalov BK, Flynn KC, Neukirchen D, Meyn L, Teusch N, Wu X, Brakebusch C, Bamburg JR, Bradke F (2007) Cdc42 regulates cofilin during the establishment of neuronal polarity. J Neurosci 27:13117–13129.

    Article  PubMed  CAS  Google Scholar 

  • Gertler FB, Doctor JS, Hoffmann FM (1990) Genetic suppression of mutations in the Drosophila abl proto-oncogene homolog. Science 248:857–860.

    Article  PubMed  CAS  Google Scholar 

  • Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, Condeelis JS (2004) Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304:743–746.

    Article  PubMed  CAS  Google Scholar 

  • Gilmore EC, Ohshima T, Goffinet AM, Kulkarni AB, Herrup K (1998) Cyclin-dependent kinase 5-deficient mice demonstrate novel developmental arrest in cerebral cortex. J Neurosci 18:6370–6377.

    PubMed  CAS  Google Scholar 

  • Goh KL, Cai L, Cepko CL, Gertler FB (2002) Ena/VASP proteins regulate cortical neuronal positioning. Curr Biol 12:565–569.

    Article  PubMed  CAS  Google Scholar 

  • Govek EE, Newey SE, Akerman CJ, Cross JR, Van der Veken L, Van Aelst L (2004) The X-linked mental retardation protein oligophrenin-1 is required for dendritic spine morphogenesis. Nat Neurosci 7:364–372.

    Article  PubMed  CAS  Google Scholar 

  • Grabham PW, Seale GE, Bennecib M, Goldberg DJ, Vallee RB (2007) Cytoplasmic dynein and LIS1 are required for microtubule advance during growth cone remodeling and fast axonal outgrowth. J Neurosci 27:5823–5834.

    Article  PubMed  CAS  Google Scholar 

  • Guerrini R, Moro F, Andermann E, Hughes E, D’Agostino D, Carrozzo R, Bernasconi A, Flinter F, Parmeggiani L, Volzone A, Parrini E, Mei D, Jarosz JM, Morris RG, Pratt P, Tortorella G, Dubeau F, Andermann F, Dobyns WB, Das S (2003) Nonsyndromic mental retardation and cryptogenic epilepsy in women with doublecortin gene mutations. Ann Neurol 54:30–37.

    Article  PubMed  Google Scholar 

  • Gupton SL, Eisenmann K, Alberts AS, Waterman-Storer CM (2007) mDia2 regulates actin and focal adhesion dynamics and organization in the lamella for efficient epithelial cell migration. J Cell Sci 120:3475–3487.

    Article  PubMed  CAS  Google Scholar 

  • Gupton SL, Waterman-Storer CM (2006) Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell 125:1361–1374.

    Article  PubMed  CAS  Google Scholar 

  • Gurniak CB, Perlas E, Witke W (2005) The actin depolymerizing factor n-cofilin is essential for neural tube morphogenesis and neural crest cell migration. Dev Biol 278:231–241.

    Article  PubMed  CAS  Google Scholar 

  • Hall A (1994) Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu Rev Cell Biol 10:31–54.

    Article  PubMed  CAS  Google Scholar 

  • Harris ES, Higgs HN (2004) Actin cytoskeleton: formins lead the way. Curr Biol 14:R520–R522.

    Article  PubMed  CAS  Google Scholar 

  • Hatten ME (1990) Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain. Trends Neurosci 13:179–184.

    Article  PubMed  CAS  Google Scholar 

  • Hirotsune S, Fleck MW, Gambello MJ, Bix GJ, Chen A, Clark GD, Ledbetter DH, McBain CJ, Wynshaw-Boris A (1998) Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat Genet 19:333–9.

    Article  PubMed  CAS  Google Scholar 

  • Hong SE, Shugart YY, Huang DT, Shahwan SA, Grant PE, Hourihane JO, Martin ND, Walsh CA (2000) Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet 26:93–96.

    Article  PubMed  CAS  Google Scholar 

  • Huang TY, DerMardirossian C, Bokoch GM (2006) Cofilin phosphatases and regulation of actin dynamics. Curr Opin Cell Biol 18:26–31.

    Article  PubMed  CAS  Google Scholar 

  • Jacobs T, Causeret F, Nishimura YV, Terao M, Norman A, Hoshino M, Nikolic M (2007) Localized activation of p21-activated kinase controls neuronal polarity and morphology. J Neurosci 27:8604–8615.

    Article  PubMed  CAS  Google Scholar 

  • Kaksonen M, Toret CP, Drubin DG (2006) Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7:404–414.

    Article  PubMed  CAS  Google Scholar 

  • Kamiguchi H, Lemmon V (2000) Recycling of the cell adhesion molecule L1 in axonal growth cones. J Neurosci 20:3676–3686.

    PubMed  CAS  Google Scholar 

  • Kawauchi T, Chihama K, Nabeshima Y, Hoshino M (2006) Cdk5 phosphorylates and stabilizes p27(kip1) contributing to actin organization and cortical neuronal migration. Nat Cell Biol 8:17–26.

    Article  PubMed  CAS  Google Scholar 

  • Kholmanskikh SS, Dobrin JS, Wynshaw-Boris A, Letourneau PC, Ross ME (2003) Disregulated RhoGTPases and actin cytoskeleton contribute to the migration defect in Lis1-deficient neurons. J Neurosci 23:8673–8681.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kim AS, Kakalis LT, Abdul-Manan N, Liu GA, Rosen MK (2000) Autoinhibition and activation mechanisms of the Wiskott–Aldrich syndrome protein. Nature 404:151–158.

    Article  PubMed  CAS  Google Scholar 

  • Ko J, Humbert S, Bronson RT, Takahashi S, Kulkarni AB, Li E, Tsai LH (2001) p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment. J Neurosci 21:6758–6771.

    PubMed  CAS  Google Scholar 

  • Krause M, Dent EW, Bear JE, Loureiro JJ, Gertler FB (2003) Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu Rev Cell Dev Biol 19:541–564.

    Article  PubMed  CAS  Google Scholar 

  • Kuczmarski ER, Rosenbaum JL (1979) Studies on the organization and localization of actin and myosin in neurons. J Cell Biol 80:356–371.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kwon YT, Tsai LH (1998) A novel disruption of cortical development in p35(–/–) mice distinct from reeler. J Comp Neurol 395:510–522.

    Article  PubMed  CAS  Google Scholar 

  • Lauffenburger DA, Horwitz AF (1996) Cell migration: a physically integrated molecular process. Cell 84:359–369.

    Article  PubMed  CAS  Google Scholar 

  • Le Clainche C, Schlaepfer D, Ferrari A, Klingauf M, Grohmanova K, Veligodskiy A, Didry D, Le D, Egile C, Carlier MF, Kroschewski R (2007) IQGAP1 stimulates actin assembly through the N-WASP-Arp2/3 pathway. J Biol Chem 282:426–435.

    Article  PubMed  CAS  Google Scholar 

  • Leventer RJ, Cardoso C, Ledbetter DH, Dobyns WB (2001) LIS1: from cortical malformation to essential protein of cellular dynamics. Trends Neurosci 24:489–492.

    Article  PubMed  CAS  Google Scholar 

  • Lindner J, Rathjen FG, Schachner M (1983) L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. Nature 305:427–430.

    Article  PubMed  CAS  Google Scholar 

  • Lo Nigro C, Chong CS, Smith AC, Dobyns WB, Carrozzo R, Ledbetter DH (1997) Point mutations and an intragenic deletion in LIS1, the lissencephaly causative gene in isolated lissencephaly sequence and Miller–Dieker syndrome. Hum Mol Genet 6:157–164.

    Article  PubMed  CAS  Google Scholar 

  • Machesky LM, Mullins RD, Higgs HN, Kaiser DA, Blanchoin L, May RC, Hall ME, Pollard TD (1999) Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc Natl Acad Sci USA 96:3739–3744.

    Article  PubMed  CAS  Google Scholar 

  • Manent JB, Represa A (2007) Neurotransmitters and brain maturation: early paracrine actions of GABA and glutamate modulate neuronal migration. Neuroscientist 13:268–279.

    Article  PubMed  CAS  Google Scholar 

  • Marin O, Rubenstein JL (2001) A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2:780–790.

    Article  PubMed  CAS  Google Scholar 

  • Marin O, Valdeolmillos M, Moya F (2006) Neurons in motion: same principles for different shapes? Trends Neurosci 29:655–661.

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto N, Leventer RJ, Kuc JA, Mewborn SK, Dudlicek LL, Ramocki MB, Pilz DT, Mills PL, Das S, Ross ME, Ledbetter DH, Dobyns WB (2001) Mutation analysis of the DCX gene and genotype/phenotype correlation in subcortical band heterotopia. Eur J Hum Genet 9:5–12.

    Article  PubMed  CAS  Google Scholar 

  • Mejillano MR, Kojima S, Applewhite DA, Gertler FB, Svitkina TM, Borisy GG (2004) Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118:363–373.

    Article  PubMed  CAS  Google Scholar 

  • Merrifield CJ, Moss SE, Ballestrem C, Imhof BA, Giese G, Wunderlich I, Almers W (1999) Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nat Cell Biol 1:72–74.

    Article  PubMed  CAS  Google Scholar 

  • Miki H, Suetsugu S, Takenawa T (1998) WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. Embo J 17:6932–6941.

    Article  PubMed  CAS  Google Scholar 

  • Millard TH, Sharp SJ, Machesky LM (2004) Signalling to actin assembly via the WASP (Wiskott–Aldrich syndrome protein)-family proteins and the Arp2/3 complex. Biochem J 380:1–17.

    Article  PubMed  CAS  Google Scholar 

  • Mitchison TJ, Cramer LP (1996) Actin-based cell motility and cell locomotion. Cell 84:371–379.

    Article  PubMed  CAS  Google Scholar 

  • Moro F, Pisano T, Bernardina BD, Polli R, Murgia A, Zoccante L, Darra F, Battaglia A, Pramparo T, Zuffardi O, Guerrini R (2006) Periventricular heterotopia in fragile X syndrome. Neurology 67:713–715.

    Article  PubMed  CAS  Google Scholar 

  • Mullins RD, Heuser JA, Pollard TD (1998) The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc Natl Acad Sci USA 95:6181–6186.

    Article  PubMed  CAS  Google Scholar 

  • Mullins RD, Pollard TD (1999) Rho-family GTPases require the Arp2/3 complex to stimulate actin polymerization in Acanthamoeba extracts. Curr Biol 9:405–415.

    Article  PubMed  CAS  Google Scholar 

  • Niewmierzycka A, Mills J, St-Arnaud R, Dedhar S, Reichardt LF (2005) Integrin-linked kinase deletion from mouse cortex results in cortical lamination defects resembling cobblestone lissencephaly. J Neurosci 25:7022–7031.

    Article  PubMed  CAS  Google Scholar 

  • Nobes CD, Hall A (1995) Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53–62.

    Article  PubMed  CAS  Google Scholar 

  • Noritake J, Watanabe T, Sato K, Wang S, Kaibuchi K (2005) IQGAP1: a key regulator of adhesion and migration. J Cell Sci 118:2085–2092.

    Article  PubMed  CAS  Google Scholar 

  • Ono S (2007) Mechanism of depolymerization and severing of actin filaments and its significance in cytoskeletal dynamics. Int Rev Cytol 258:1–82.

    Article  PubMed  CAS  Google Scholar 

  • Orth JD, Krueger EW, Cao H, McNiven MA (2002) The large GTPase dynamin regulates actin comet formation and movement in living cells. Proc Natl Acad Sci USA 99:167–172.

    Article  PubMed  CAS  Google Scholar 

  • Panicker AK, Buhusi M, Erickson A, Maness PF (2006) Endocytosis of beta1 integrins is an early event in migration promoted by the cell adhesion molecule L1. Exp Cell Res 312:299–307.

    PubMed  CAS  Google Scholar 

  • Parrini E, Ramazzotti A, Dobyns WB, Mei D, Moro F, Veggiotti P, Marini C, Brilstra EH, Dalla Bernardina B, Goodwin L, Bodell A, Jones MC, Nangeroni M, Palmeri S, Said E, Sander JW, Striano P, Takahashi Y, Van Maldergem L, Leonardi G, Wright M, Walsh CA, Guerrini R (2006) Periventricular heterotopia: phenotypic heterogeneity and correlation with filamin A mutations. Brain 129:1892–1906.

    Article  PubMed  CAS  Google Scholar 

  • Pellegrin S, Mellor H (2005) The Rho family GTPase Rif induces filopodia through mDia2. Curr Biol 15:129–133.

    Article  PubMed  CAS  Google Scholar 

  • Peng J, Wallar BJ, Flanders A, Swiatek PJ, Alberts AS (2003) Disruption of the Diaphanous-related formin Drf1 gene encoding mDia1 reveals a role for Drf3 as an effector for Cdc42. Curr Biol 13:534–545.

    Article  PubMed  CAS  Google Scholar 

  • Philip N, Chabrol B, Lossi AM, Cardoso C, Guerrini R, Dobyns WB, Raybaud C, Villard L (2003) Mutations in the oligophrenin-1 gene (OPHN1) cause X linked congenital cerebellar hypoplasia. J Med Genet 40:441–446.

    Article  PubMed  CAS  Google Scholar 

  • Pollard TD (2003) The cytoskeleton, cellular motility and the reductionist agenda. Nature 422:741–745.

    Article  PubMed  CAS  Google Scholar 

  • Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453–465.

    Article  PubMed  CAS  Google Scholar 

  • Proux-Gillardeaux V, Raposo G, Irinopoulou T, Galli T (2007) Expression of the Longin domain of TI-VAMP impairs lysosomal secretion and epithelial cell migration. Biol Cell 99:261–271.

    Article  PubMed  CAS  Google Scholar 

  • Rakic P (1971) Neuron–glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electron microscopic study in Macacus rhesus. J Comp Neurol 141:283–312.

    Article  PubMed  CAS  Google Scholar 

  • Ridley AJ, Hall A (1992) Signal transduction pathways regulating rho-mediated stress fiber formation: requirement for a tyrosine kinase. EMBO J 13:2600–2610.

    Google Scholar 

  • Rivas RJ, Hatten ME (1995) Motility and cytoskeletal organization of migrating cerebellar granule neurons. J Neurosci 15:981–989.

    PubMed  CAS  Google Scholar 

  • Rodriguez OC, Schaefer AW, Mandato CA, Forscher P, Bement WM, Waterman-Storer CM (2003) Conserved microtubule–actin interactions in cell movement and morphogenesis. Nat Cell Biol 5:599–609.

    Article  PubMed  CAS  Google Scholar 

  • Ross ME, Swanson K, Dobyns WB (2001) Lissencephaly with cerebellar hypoplasia (LCH): a heterogeneous group of cortical malformations. Neuropediatrics 32:256–263.

    Article  PubMed  CAS  Google Scholar 

  • Sachdev P, Menon S, Kastner DB, Chuang JZ, Yeh TY, Conde C, Caceres A, Sung CH, Sakmar TP (2007) G protein beta gamma subunit interaction with the dynein light-chain component Tctex-1 regulates neurite outgrowth. Embo J 26:2621–2632.

    Article  PubMed  CAS  Google Scholar 

  • Sapir T, Shmueli A, Levy T, Timm T, Elbaum M, Mandelkow EM, Reiner O. (2008) Antagonistic effects of doublecortin and MARK2/Par-1 in the developing cerebral cortex. J Neurosci 28:13008–13.

    PubMed  Google Scholar 

  • Schaar BT, McConnell SK (2005) Cytoskeletal coordination during neuronal migration. Proc Natl Acad Sci USA 102:13652–13657.

    Article  PubMed  CAS  Google Scholar 

  • Schenck A, Bardoni B, Langmann C, Harden N, Mandel JL, Giangrande A (2003) CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron 38:887–898.

    Article  PubMed  CAS  Google Scholar 

  • Schirenbeck A, Arasada R, Bretschneider T, Stradal TE, Schleicher M, Faix J (2006) The bundling activity of vasodilator-stimulated phosphoprotein is required for filopodium formation. Proc Natl Acad Sci USA 103:7694–7699.

    Article  PubMed  CAS  Google Scholar 

  • Schirenbeck A, Bretschneider T, Arasada R, Schleicher M, Faix J (2005) The Diaphanous-related formin dDia2 is required for the formation and maintenance of filopodia. Nat Cell Biol 7:619–625.

    Article  PubMed  CAS  Google Scholar 

  • Schlessinger K, McManus EJ, Hall A (2007) Cdc42 and noncanonical Wnt signal transduction pathways cooperate to promote cell polarity. J Cell Biol 178:355–361.

    Article  PubMed  CAS  Google Scholar 

  • Schmid RS, Jo R, Shelton S, Kreidberg JA, Anton ES (2005) Reelin, integrin and DAB1 interactions during embryonic cerebral cortical development. Cereb Cortex 15:1632–1636.

    Article  PubMed  Google Scholar 

  • Schmid RS, Shelton S, Stanco A, Yokota Y, Kreidberg JA, Anton ES (2004) alpha3beta1 integrin modulates neuronal migration and placement during early stages of cerebral cortical development. Development 131:6023–6031.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Sheldon M, Rice DS, D’Arcangelo G, Yoneshima H, Nakajima K, Mikoshiba K, Howell BW, Cooper JA, Goldowitz D, Curran T (1997) Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389:730–733.

    Article  PubMed  CAS  Google Scholar 

  • Shu T, Ayala R, Nguyen MD, Xie Z, Gleeson JG, Tsai LH (2004) Ndel1 operates in a common pathway with LIS1 and cytoplasmic dynein to regulate cortical neuronal positioning. Neuron 44:263–277.

    Article  PubMed  CAS  Google Scholar 

  • Shupliakov O, Bloom O, Gustafsson JS, Kjaerulff O, Low P, Tomilin N, Pieribone VA, Greengard P, Brodin L (2002) Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton. Proc Natl Acad Sci USA 99:14476–14481.

    Article  PubMed  CAS  Google Scholar 

  • Sisodiya SM, Thom M, Lin WR, Bajaj NP, Cross JH, Harding BN (2002) Abnormal expression of cdk5 in focal cortical dysplasia in humans. Neurosci Lett 328:217–220.

    Article  PubMed  CAS  Google Scholar 

  • Solecki DJ, Govek EE, Tomoda T, Hatten ME (2006) Neuronal polarity in CNS development. Genes Dev 20:2639–2647.

    Article  PubMed  CAS  Google Scholar 

  • Solecki DJ, Model L, Gaetz J, Kapoor TM, Hatten ME (2004) Par6alpha signaling controls glial-guided neuronal migration. Nat Neurosci 7:1195–1203.

    Article  PubMed  Google Scholar 

  • Southwick FS (2000) Gelsolin and ADF/cofilin enhance the actin dynamics of motile cells. Proc Natl Acad Sci USA 97:6936–6938.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Takenawa T, Suetsugu S (2007) The WASP–WAVE protein network: connecting the membrane to the cytoskeleton. Nat Rev Mol Cell Biol 8:37–48.

    Article  PubMed  CAS  Google Scholar 

  • Tanaka T, Serneo FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG (2004a) Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 165:709–721.

    Article  PubMed  CAS  Google Scholar 

  • Tanaka T, Serneo FF, Tseng HC, Kulkarni AB, Tsai LH, Gleeson JG (2004b) Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron 41:215–227.

    Article  PubMed  CAS  Google Scholar 

  • Thelen K, Kedar V, Panicker AK, Schmid RS, Midkiff BR, Maness PF (2002) The neural cell adhesion molecule L1 potentiates integrin-dependent cell migration to extracellular matrix proteins. J Neurosci 22:4918–4931.

    PubMed  CAS  Google Scholar 

  • Theriot JA, Mitchison TJ (1993) The three faces of profilin. Cell 75:835–838.

    Article  PubMed  CAS  Google Scholar 

  • Tomasiewicz H, Ono K, Yee D, Thompson C, Goridis C, Rutishauser U, Magnuson T (1993) Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11:1163–1174.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Tsai JW, Bremner KH, Vallee RB (2007) Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nat Neurosci 10:970–979.

    Article  PubMed  CAS  Google Scholar 

  • Tsai LH, Gleeson JG (2005) Nucleokinesis in neuronal migration. Neuron 46:383–388.

    Article  PubMed  CAS  Google Scholar 

  • Tsukada M, Prokscha A, Ungewickell E, Eichele G (2005) Doublecortin association with actin filaments is regulated by neurabin II. J Biol Chem 280:11361–11368.

    Article  PubMed  CAS  Google Scholar 

  • Wang S, Watanabe T, Noritake J, Fukata M, Yoshimura T, Itoh N, Harada T, Nakagawa M, Matsuura Y, Arimura N, Kaibuchi K (2007) IQGAP3, a novel effector of Rac1 and Cdc42, regulates neurite outgrowth. J Cell Sci 120:567–577.

    Article  PubMed  CAS  Google Scholar 

  • Watanabe N, Madaule P, Reid T, Ishizaki T, Watanabe G, Kakizuka A, Saito Y, Nakao K, Jockusch BM, Narumiya S (1997) p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. Embo J 16:3044–3056.

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T, Wang S, Noritake J, Sato K, Fukata M, Takefuji M, Nakagawa M, Izumi N, Akiyama T, Kaibuchi K (2004) Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev Cell 7:871–883.

    Article  PubMed  CAS  Google Scholar 

  • Withee J, Galligan B, Hawkins N, Garriga G (2004) Caenorhabditis elegans WASP and Ena/VASP proteins play compensatory roles in morphogenesis and neuronal cell migration. Genetics 167:1165–1176.

    Article  PubMed  CAS  Google Scholar 

  • Wong EV, Kenwrick S, Willems P, Lemmon V (1995) Mutations in the cell adhesion molecule L1 cause mental retardation. Trends Neurosci 18:168–172.

    Article  PubMed  CAS  Google Scholar 

  • Xie Z, Samuels BA, Tsai LH (2006) Cyclin-dependent kinase 5 permits efficient cytoskeletal remodeling–a hypothesis on neuronal migration. Cereb Cortex 16(Suppl 1):i64–i68.

    Article  PubMed  Google Scholar 

  • Xie Z, Sanada K, Samuels BA, Shih H, Tsai LH (2003) Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 114:469–482.

    Article  PubMed  CAS  Google Scholar 

  • Xie Z, Tsai LH (2004) Cdk5 phosphorylation of FAK regulates centrosome-associated miocrotubules and neuronal migration. Cell Cycle 3:108–110.

    PubMed  CAS  Google Scholar 

  • Yarar D, Waterman-Storer CM, Schmid SL (2005) A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 16:964–975.

    Article  PubMed  CAS  Google Scholar 

  • Yarmola EG, Bubb MR (2004) Effects of profilin and thymosin beta4 on the critical concentration of actin demonstrated in vitro and in cell extracts with a novel direct assay. J Biol Chem 279:33519–33527.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Elizabeth Ross .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Ross, M.E., Kholmanskikh, S. (2011). Actin Cytoskeletal Regulation in Neuronal Migration. In: Gallo, G., Lanier, L. (eds) Neurobiology of Actin. Advances in Neurobiology, vol 5. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-7368-9_8

Download citation

Publish with us

Policies and ethics