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Actin and Neuronal Polarity

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Book cover Neurobiology of Actin

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

Abstract

Mechanisms determining neuronal polarity have been most extensively studied using dissociated hippocampal neurons which develop in a very stereotypic manner in the absence of differential extrinsic cues. Polarity is established in two major steps: first, an initial deformation of the spherical cell gives rise to the first neurite, and later, after multiple neurites grew from the sphere, one neurite will be selected for fast axonal outgrowth. Both steps are under the tight control of cytoskeletal rearrangements; sub-membranous local actin remodelling will support the disruption of the spherical architecture to thus allow the formation of the first neurite and from this, later on, rapid growth. Axonal growth from a multipolar neuron at later stages has been shown to be supported by local actin destabilization and that could be achieved either by intrinsic or extrinsic cues, demonstrating that polarity establishment is a complex endogenously controlled remodelling process, under active control by extrinsic factors.

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References

  • Aizawa H, Wakatsuki S, Ishii A, Moriyama K, Sasaki Y, Ohashi K, Sekine-Aizawa Y, Sehara-Fujisawa A, Mizuno K, Goshima Y, Yahara I (2001) Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse. Nat Neurosci 4:367–373.

    Article  PubMed  CAS  Google Scholar 

  • Arimura N, Kaibuchi K (2007) Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat Rev Neurosci 8:194–205.

    Article  PubMed  CAS  Google Scholar 

  • Bagnard D, Lohrum M, Uziel D, Puschel AW, Bolz J (1998) Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections. Development 125:5043–5053.

    PubMed  CAS  Google Scholar 

  • Bernards A, Settleman J (2004) GAP control: regulating the regulators of small GTPases. Trends Cell Biol 14:377–385.

    Article  PubMed  CAS  Google Scholar 

  • Bito H, Furuyashiki T, Ishihara H, Shibasaki Y, Ohashi K, Mizuno K, Maekawa M, Ishizaki T, Narumiya S (2000) A critical role for a Rho-associated kinase, p160ROCK, in determining axon outgrowth in mammalian CNS neurons. Neuron 26:431–441.

    Article  PubMed  CAS  Google Scholar 

  • Bradke F, Dotti CG (1997) Neuronal polarity: vectorial cytoplasmic flow precedes axon formation. Neuron 19:1175–1186.

    Article  PubMed  CAS  Google Scholar 

  • Bradke F, Dotti CG (1999) The role of local actin instability in axon formation. Science 283:1931–1934.

    Article  PubMed  CAS  Google Scholar 

  • Bradke F, Dotti CG (2000) Establishment of neuronal polarity: lessons from cultured hippocampal neurons. Curr Opin Neurobiol 10:574–581.

    Article  PubMed  CAS  Google Scholar 

  • Craig AM, Banker G (1994) Neuronal polarity. Annu Rev Neurosci 17:267–310.

    Article  PubMed  CAS  Google Scholar 

  • Da Silva JS, Medina M, Zuliani C, Di Nardo A, Witke W, Dotti CG (2003) RhoA/ROCK regulation of neuritogenesis via profilin IIa-mediated control of actin stability. J Cell Biol 162:1267–1279.

    Article  PubMed  CAS  Google Scholar 

  • de Anda FC, Pollarolo G, Da Silva JS, Camoletto PG, Feiguin F, Dotti CG (2005) Centrosome localization determines neuronal polarity. Nature 436:704–708.

    Article  PubMed  CAS  Google Scholar 

  • Dent EW, Gertler FB (2003) Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40:209–227.

    Article  PubMed  CAS  Google Scholar 

  • Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454–1468.

    PubMed  CAS  Google Scholar 

  • Esch T, Lemmon V, Banker G (1999) Local presentation of substrate molecules directs axon specification by cultured hippocampal neurons. J Neurosci 19:6417–6426.

    PubMed  CAS  Google Scholar 

  • Forscher P, Smith SJ (1988) Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J Cell Biol 107:1505–1516.

    Article  PubMed  CAS  Google Scholar 

  • Gallo G, Letourneau PC (2004) Regulation of growth cone actin filaments by guidance cues. J Neurobiol 58:92–102.

    Article  PubMed  CAS  Google Scholar 

  • Gotz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777–788.

    Article  PubMed  CAS  Google Scholar 

  • Grabham PW, Reznik B, Goldberg DJ (2003) Microtubule and Rac 1-dependent F-actin in growth cones. J Cell Sci 116:3739–3748.

    Article  PubMed  CAS  Google Scholar 

  • Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279:509–514.

    Article  PubMed  CAS  Google Scholar 

  • Hatten ME (1999) Central nervous system neuronal migration. Annu Rev Neurosci 22:511–539.

    Article  PubMed  CAS  Google Scholar 

  • Horton AC, Ehlers MD (2003) Neuronal polarity and trafficking. Neuron 40:277–295.

    Article  PubMed  CAS  Google Scholar 

  • Inagaki N, Chihara K, Arimura N, Menager C, Kawano Y, Matsuo N, Nishimura T, Amano M, Kaibuchi K (2001) CRMP-2 induces axons in cultured hippocampal neurons. Nat Neurosci 4:781–782.

    Article  PubMed  CAS  Google Scholar 

  • Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–269.

    Article  PubMed  CAS  Google Scholar 

  • Kriegstein AR, Noctor SC (2004) Patterns of neuronal migration in the embryonic cortex. Trends Neurosci 27:392–399.

    Article  PubMed  CAS  Google Scholar 

  • Kunda P, Paglini G, Quiroga S, Kosik K, Caceres A (2001) Evidence for the involvement of Tiam1 in axon formation. J Neurosci 21:2361–2372.

    PubMed  CAS  Google Scholar 

  • Lefcort F, Bentley D (1989) Organization of cytoskeletal elements and organelles preceding growth cone emergence from an identified neuron in situ. J Cell Biol 108:1737–1749.

    Article  PubMed  CAS  Google Scholar 

  • Lochter A, Schachner M (1993) Tenascin and extracellular matrix glycoproteins: from promotion to polarization of neurite growth in vitro. J Neurosci 13:3986–4000.

    PubMed  CAS  Google Scholar 

  • Luo L (2000) Rho GTPases in neuronal morphogenesis. Nat Rev Neurosci 1:173–180.

    Article  PubMed  CAS  Google Scholar 

  • Morales M, Colicos MA, Goda Y (2000) Actin-dependent regulation of neurotransmitter release at central synapses. Neuron 27:539–550.

    Article  PubMed  CAS  Google Scholar 

  • Muallem S, Kwiatkowska K, Xu X, Yin HL (1995) Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J Cell Biol 128:589–598.

    Article  PubMed  CAS  Google Scholar 

  • Nadarajah B, Alifragis P, Wong RO, Parnavelas JG (2003) Neuronal migration in the developing cerebral cortex: observations based on real-time imaging. Cereb Cortex 13:607–611.

    Article  PubMed  CAS  Google Scholar 

  • Nakamura F, Kalb RG, Strittmatter SM (2000) Molecular basis of semaphorin-mediated axon guidance. J Neurobiol 44:219–229.

    Article  PubMed  CAS  Google Scholar 

  • Nelson WJ (2003) Adaptation of core mechanisms to generate cell polarity. Nature 422:766–774.

    Article  PubMed  CAS  Google Scholar 

  • Ng J, Luo L (2004) Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron 44:779–793.

    Article  PubMed  CAS  Google Scholar 

  • Nishimura T, Yamaguchi T, Kato K, Yoshizawa M, Nabeshima Y, Ohno S, Hoshino M, Kaibuchi K (2005) PAR-6-PAR-3 mediates Cdc42-induced Rac activation through the Rac GEFs STEF/Tiam1. Nat Cell Biol 7:270–277.

    Article  PubMed  CAS  Google Scholar 

  • Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7:136–144.

    Article  PubMed  CAS  Google Scholar 

  • Olofsson B (1999) Rho guanine dissociation inhibitors: pivotal molecules in cellular signalling. Cell Signal 11:545–554.

    Article  PubMed  CAS  Google Scholar 

  • Parnavelas JG, Alifragis P, Nadarajah B (2002) The origin and migration of cortical neurons. Prog Brain Res 136:73–80.

    Article  PubMed  Google Scholar 

  • Polleux F, Giger RJ, Ginty DD, Kolodkin AL, Ghosh A (1998) Patterning of cortical efferent projections by semaphorin–neuropilin interactions. Science 282:1904–1906.

    Article  PubMed  CAS  Google Scholar 

  • Polleux F, Morrow T, Ghosh A (2000) Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404:567–573.

    Article  PubMed  CAS  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 

  • Rosso S, Bollati F, Bisbal M, Peretti D, Sumi T, Nakamura T, Quiroga S, Ferreira A, Caceres A (2004) LIMK1 regulates Golgi dynamics, traffic of Golgi-derived vesicles, and process extension in primary cultured neurons. Mol Biol Cell 15:3433–3449.

    Article  PubMed  CAS  Google Scholar 

  • Ruthel G, Hollenbeck PJ (2000) Growth cones are not required for initial establishment of polarity or differential axon branch growth in cultured hippocampal neurons. J Neurosci 20:k2266–2274.

    PubMed  CAS  Google Scholar 

  • Schmidt A, Hall A (2002) Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev 16:1587–1609.

    Article  PubMed  CAS  Google Scholar 

  • Schwamborn JC, Muller M, Becker AH, Puschel AW (2007) Ubiquitination of the GTPase Rap1B by the ubiquitin ligase Smurf2 is required for the establishment of neuronal polarity. EMBO J 26:1410–1422.

    Article  PubMed  CAS  Google Scholar 

  • Schwamborn JC, Puschel AW (2004) The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat Neurosci 7:923–929.

    Article  PubMed  CAS  Google Scholar 

  • Shoukimas GM, Hinds JW (1978) The development of the cerebral cortex in the embryonic mouse: an electron microscopic serial section analysis. J Comp Neurol 179:795–830.

    Article  PubMed  CAS  Google Scholar 

  • Skaliora I, Singer W, Betz H, Puschel AW (1998) Differential patterns of semaphorin expression in the developing rat brain. Eur J Neurosci 10:1215–1229.

    Article  PubMed  CAS  Google Scholar 

  • Smythe E, Ayscough KR (2006) Actin regulation in endocytosis. J Cell Sci 119:4589–4598.

    Article  PubMed  CAS  Google Scholar 

  • Tabata H, Nakajima K (2003) Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J Neurosci 23:9996–10001.

    PubMed  CAS  Google Scholar 

  • Uchida Y, Ohshima T, Sasaki Y, Suzuki H, Yanai S, Yamashita N, Nakamura F, Takei K, Ihara Y, Mikoshiba K et al. (2005) Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3beta phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer’s disease. Genes Cells 10:165–179.

    Article  PubMed  CAS  Google Scholar 

  • Venstrom KA, Reichardt LF (1993) Extracellular matrix. 2: role of extracellular matrix molecules and their receptors in the nervous system. Faseb J 7:996–1003.

    PubMed  CAS  Google Scholar 

  • Watabe-Uchida M, John KA, Janas JA, Newey SE, Van Aelst L (2006) The Rac activator DOCK7 regulates neuronal polarity through local phosphorylation of stathmin/Op18. Neuron 51:727–739.

    Article  PubMed  CAS  Google Scholar 

  • Waterman-Storer CM, Salmon E (1999) Positive feedback interactions between microtubule and actin dynamics during cell motility. Curr Opin Cell Biol 11:61–67.

    Article  PubMed  CAS  Google Scholar 

  • Wiesner S, Lange A, Fassler R (2006) Local call: from integrins to actin assembly. Trends Cell Biol 16:327–329.

    Article  PubMed  CAS  Google Scholar 

  • Wiesner S, Legate KR, Fassler R (2005) Integrin–actin interactions. Cell Mol Life Sci 62:1081–1099.

    Article  PubMed  CAS  Google Scholar 

  • Wiggin GR, Fawcett JP, Pawson T (2005) Polarity proteins in axon specification and synaptogenesis. Dev Cell 8:803–816.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. VIB, Department of Molecular and Developmental Genetics and Department of Human Genetics, Catholic University of Leuven, 3000, Leuven, Belgium

    Annette Gärtner & Carlos G. Dotti

Authors
  1. Annette Gärtner
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  2. Carlos G. Dotti
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Correspondence to Carlos G. Dotti .

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Editors and Affiliations

  1. , Dept Neurobiology and Anatomy, Drexel University College of Medicine, 2900 Queen Lane, Philadelphia, 19129, Pennsylvania, USA

    Gianluca Gallo

  2. 4-140 MCB, Department of Neuroscience, University of Minnesota, 321 Church St., Minneapolis, 55455, Minnesota, USA

    Lorene M. Lanier

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Gärtner, A., Dotti, C.G. (2011). Actin and Neuronal Polarity. 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_9

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