Skip to main content
SpringerLink
Log in

Regulation of Actin Filaments During Neurite Extension and Guidance

  • Chapter
  • First Online:
Neurobiology of Actin

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

  • 796 Accesses

Abstract

Behavior and other neural functions are based on neural circuits that develop over a prolonged period, which lasts in humans from the second fetal month through postnatal years. These circuits develop as neurons extend complex cytoplasmic processes, long axons and highly branched dendrites, expressing intrinsic morphogenetic behaviors while interacting with other cells and molecules of the developing organism. Actin-based motility dominates this morphogenetic process of developing neural circuits. Actin, always one of the most abundant intracellular proteins in neurons, is expressed at its highest levels during neuronal morphogenesis (Santerre and Rich 1976). An analysis of the actin content of embryonic sympathetic neurons indicated that actin comprises up to 20% of total cell protein (Fine and Bray 1971). Much of this actin is used in the motility that drives the formation of axons and dendrites. This chapter describes the roles of actin in the intrinsic mechanisms of morphogenesis of axons and dendrites and the extrinsic environmental features that regulate where and when axons and dendrites grow.

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

Access this chapter

Log in via an institution
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

  • Adler C, Fetter R, Bargmann C (2006) UNC-6/Netrin induces neuronal asymmetry and defines the site of axon formation. Nat Neurosci 9:511–518.

    Article  PubMed  CAS  Google Scholar 

  • Arimura N, Kaibuchi K (2005) Key regulators in neuronal polarity. Neuron 48:881–884.

    Article  PubMed  CAS  Google Scholar 

  • Baas PW, Buster DW (2004) Slow axonal transport and the genesis of neuronal morphology. J Neurobiol 58:3–17.

    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 

  • Bagri A, Marín O, Plump AS, Mak J, Pleasure SJ, Rubenstein JLR, Tessier-Lavigne M (2002) Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 33:233–248.

    Article  PubMed  CAS  Google Scholar 

  • Bisby M, Tetzlaff W (1992) Changes in cytoskeletal protein synthesis following axon injury and during axon regeneration. Mol Neurobiol 6:107–123.

    Article  PubMed  CAS  Google Scholar 

  • Blackmore M, Letourneau P (2006) Changes within maturing neurons limit axonal regeneration in the developing spinal cord. J Neurobiol 66:348–360.

    Article  PubMed  CAS  Google Scholar 

  • Blackmore M, Letourneau PC (2007) Protein synthesis in distal axons is not required for axon growth in the embryonic spinal cord. Dev Neurobiol 67:976–986.

    Article  PubMed  CAS  Google Scholar 

  • Braisted JE, Catalano SM, Stimac R, Kennedy TE, Tessier-Lavigne M, Shatz CJ, O’Leary DD (2000) Netrin-1 promotes thalamic axon growth and is required for proper development of the thalamocortical projection. J Neurosci 20:5792–5801.

    PubMed  CAS  Google Scholar 

  • Brittis PA, Lu Q, Flanagan JG (2002) Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110:223–235.

    Article  PubMed  CAS  Google Scholar 

  • Brown ME, Bridgman PC (2004) Myosin function in nervous and sensory systems. J Neurobiol 58:118–130.

    Article  PubMed  CAS  Google Scholar 

  • Challacombe JF, Snow DM, Letourneau PC (1997) Dynamic microtubule ends are required for growth cone turning to avoid an inhibitory guidance cue. J Neurosci 17:3085–3095.

    PubMed  CAS  Google Scholar 

  • Chierzi S, Ratto GM, Verma P, Fawcett JW (2005) The ability of axons to regenerate their growth cones depends on axonal type and age, and is regulated by calcium, cAMP and ERK. Eur J Neurosci 21:2051–2062.

    Article  PubMed  Google Scholar 

  • da Silva J, Dotti C (2002) Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat Rev Neurosci 3:694–704.

    Article  PubMed  CAS  Google Scholar 

  • Dehmelt L, Halpain S (2004) Actin and microtubules in neurite initiation: are MAPs the missing link? J Neurobiol 58:18–33.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dickson B (2002) Molecular mechanisms of axon guidance. Science 298:1959–1964.

    Article  PubMed  CAS  Google Scholar 

  • Fass JN, Odde DJ (2003) Tensile force-dependent neurite elicitation via anti-beta1 integrin antibody-coated magnetic beads. Biophys J 85:623–636.

    Article  PubMed  CAS  Google Scholar 

  • Filbin MT (2006) Recapitulate development to promote axonal regeneration: good or bad approach? Philos Trans R Soc Lond B Biol Sci 361:1565–1574.

    Article  PubMed  CAS  Google Scholar 

  • Fine RE, Bray D (1971) Actin in growing nerve cells. Nat New Biol 234:115–118.

    Article  PubMed  CAS  Google Scholar 

  • Flanagan JG (2006) Neural map specification by gradients. Curr Opin Neurobiol 16:59–66.

    Article  PubMed  CAS  Google Scholar 

  • Gallo G, Letourneau P (1998) Localized sources of neurotrophins initiate axon collateral sprouting. J Neurosci 18:5403–5414.

    PubMed  CAS  Google Scholar 

  • Gallo G, Letourneau P (1999) Different contributions of microtubule dynamics and transport to the growth of axons and collateral sprouts. J Neurosci 19:3860–3873.

    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 

  • Gao PP, Yue Y, Zhang JH, Cerretti DP, Levitt P, Zhou R (1998) Regulation of thalamic neurite outgrowth by the Eph ligand ephrin-A5: implications in the development of thalamocortical projections. Proc Natl Acad Sci USA 95:5329–5334.

    Article  PubMed  CAS  Google Scholar 

  • Goldberg DJ, Burmeister DW (1986) Stages in axon formation: observations of growth of Aplysia axons in culture using video-enhanced contrast-differential interference contrast microscopy. J Cell Biol 103:1921–1931.

    Article  PubMed  CAS  Google Scholar 

  • Gomez T, Zheng J (2006) The molecular basis for calcium-dependent axon pathfinding. Nat Rev Neurosci 7:115–125.

    Article  PubMed  CAS  Google Scholar 

  • Gordon-Weeks P (2000) Neuronal Growth Cones. Cambridge University Press, Cambridge, UK.

    Book  Google Scholar 

  • Guan K, Rao Y (2003) Signalling mechanisms mediating neuronal responses to guidance cues. Nat Rev Neurosci 4:941–956.

    Article  PubMed  CAS  Google Scholar 

  • Hirokawa N, Takemura R (2004) Molecular motors in neuronal development, intracellular transport and diseases. Curr Opin Neurobiol 14:564–573.

    Article  PubMed  CAS  Google Scholar 

  • Innocenti GM, Price DJ (2005) Exuberance in the development of cortical networks. Nat Rev Neurosci 6:955–965.

    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 

  • Lamoureux P, Buxbaum RE, Heidemann SR (1989) Direct evidence that growth cones pull. Nature 340:159–162.

    Article  PubMed  CAS  Google Scholar 

  • Letourneau P (1979) Cell-substratum adhesion of neurite growth cones, and its role in neurite elongation. Exp Cell Res 124:127–138.

    Article  PubMed  CAS  Google Scholar 

  • Letourneau P (1981) Immunocytochemical evidence for colocalization in neurite growth cones of actin and myosin and their relationship to cell-substratum adhesions. Dev Biol 85:113–122.

    Article  PubMed  CAS  Google Scholar 

  • Letourneau P (1982) Analysis of microtubule number and length in cytoskeletons of cultured chick sensory neurons. J Neurosci 2:806–814.

    PubMed  CAS  Google Scholar 

  • Letourneau P (1983) Differences in the organization of actin in the growth cones compared with the neurites of cultured neurons from chick embryos. J Cell Biol 97:963–973.

    Article  PubMed  CAS  Google Scholar 

  • Letourneau PC, Shattuck TA, Ressler AH (1987) “Pull” and “push” in neurite elongation: observations on the effects of different concentrations of cytochalasin B and taxol. Cell Motil Cytoskeleton 8:193–209.

    Article  PubMed  CAS  Google Scholar 

  • Luo L (2002) Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annu Rev Cell Dev Biol 18:601–635.

    Article  PubMed  CAS  Google Scholar 

  • Mackarehtschian K, Lau CK, Caras I, McConnell SK (1999) Regional differences in the developing cerebral cortex revealed by ephrin-A5 expression. Cereb Cortex 9:601–610.

    Article  PubMed  CAS  Google Scholar 

  • Mandell JW, Banker GA (1996) Microtubule-associated proteins, phosphorylation gradients, and the establishment of neuronal polarity. Perspect Dev Neurobiol 4:125–135.

    PubMed  CAS  Google Scholar 

  • Mclaughlin T, O’Leary DDM (2005) Molecular gradients and development of retinotopic maps. Annu Rev Neurosci 28:327–355.

    Article  PubMed  CAS  Google Scholar 

  • Pearse DD, Bunge MB (2006) Designing cell- and gene-based regeneration strategies to repair the injured spinal cord. J Neurotrauma 23:438–452.

    Article  PubMed  CAS  Google Scholar 

  • Pfenninger K (1986) Of nerve growth cones, leukocytes and memory, second messenger systems and growth-related proteins. Trends Neurosci 9:562–565.

    Article  CAS  Google Scholar 

  • Pollard T, Borisy G (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 113:549.

    Article  CAS  Google Scholar 

  • Ramakers GJA (2005) Neuronal network formation in human cerebral cortex. Prog Brain Res 147:1–14.

    Article  PubMed  Google Scholar 

  • Richards LJ (2002) Axonal pathfinding mechanisms at the cortical midline and in the development of the corpus callosum. Braz J Med Biol Res 35:1431–1439.

    Article  PubMed  CAS  Google Scholar 

  • Rochlin M, Itoh K, Adelstein R, Bridgman P (1995) Localization of myosin II A and B isoforms in cultured neurons. J Cell Sci 108(Pt 12):3661–3670.

    PubMed  CAS  Google Scholar 

  • Rodriguez O, Schaefer A, Mandato C, Forscher P, Bement W, Waterman-Storer C (2003) Conserved microtubule–actin interactions in cell movement and morphogenesis. Nat Cell Biol 5:599–609.

    Article  PubMed  CAS  Google Scholar 

  • Sandvig A, Berry M, Barrett LB, Butt A, Logan A (2004) Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: expression, receptor signaling, and correlation with axon regeneration. Glia 46:225–251.

    Article  PubMed  Google Scholar 

  • Santerre RF, Rich A (1976) Actin accumulation in developing chick brain and other tissues. Dev Biol 54:1–12.

    Article  PubMed  CAS  Google Scholar 

  • Schaefer A, Kabir N, Forscher P (2002) Filopodia and actin arcs guide the assembly and transport of two populations of microtubules with unique dynamic parameters in neuronal growth cones. J Cell Biol 158:139–152.

    Article  PubMed  CAS  Google Scholar 

  • Song H, Poo M (2001) The cell biology of neuronal navigation. Nat Cell Biol 3:E81–E88.

    Article  PubMed  CAS  Google Scholar 

  • Suter DM, Forscher P (2000) Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J Neurobiol 44:97–113.

    Article  PubMed  CAS  Google Scholar 

  • Tanaka E, Ho T, Kirschner MW (1995) The role of microtubule dynamics in growth cone motility and axonal growth. J Cell Biol 128:139–155.

    Article  PubMed  CAS  Google Scholar 

  • Tanaka E, Kirschner MW (1995) The role of microtubules in growth cone turning at substrate boundaries. J Cell Biol 128:127–137.

    Article  PubMed  CAS  Google Scholar 

  • Tessier-Lavigne M, Goodman C (1996) The molecular biology of axon guidance. Science 274:1123–1133.

    Article  PubMed  CAS  Google Scholar 

  • Twiss JL, van Minnen J (2006) New insights into neuronal regeneration: the role of axonal protein synthesis in pathfinding and axonal extension. J Neurotrauma 23:295–308.

    Article  PubMed  Google Scholar 

  • Uziel D, Garcez P, Lent R, Peuckert C, Niehage R, Weth F, Bolz J (2006) Connecting thalamus and cortex: the role of ephrins. Anat Rec A Discov Mol Cell Evol Biol 288:135–142.

    PubMed  Google Scholar 

  • Van Aelst L, Cline HT (2004) Rho GTPases and activity-dependent dendrite development. Curr Opin Neurobiol 14:297–304.

    Article  PubMed  CAS  Google Scholar 

  • Vanderhaeghen P, Lu Q, Prakash N, Frisen J, Walsh CA, Frostig RD, Flanagan JG (2000) A mapping label required for normal scale of body representation in the cortex. Nat Neurosci 3:358–365.

    Article  PubMed  CAS  Google Scholar 

  • Whitford KL, Dijkhuizen P, Polleux F, Ghosh A (2002) Molecular control of cortical dendrite development. Annu Rev Neurosci 25:127–149.

    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 

  • Yamada KM, Spooner BS, Wessells NK (1971) Ultrastructure and function of growth cones and axons of cultured nerve cells. J Cell Biol 49:614–635.

    Article  PubMed  CAS  Google Scholar 

  • Zamir E, Geiger B (2001) Molecular complexity and dynamics of cell-matrix adhesions. J Cell Sci 114:3583–3590.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The author thanks the members of his laboratory who have been dedicated and enthusiastic in research on axonal growth and guidance for 30 years. The author’s research has been supported by the National Institutes of Health, National Science Foundation, and the Minnesota Medical Foundation.

Author information

Authors and Affiliations

  1. Department of Neuroscience, University of Minnesota, Minneapolis, MN, 55455, USA

    Paul Letourneau

Authors
  1. Paul Letourneau
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paul Letourneau .

Editor information

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

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Letourneau, P. (2011). Regulation of Actin Filaments During Neurite Extension and Guidance. 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_3

Download citation

Publish with us

Policies and ethics

Search

Navigation