Cytoskeletal remodeling during growth cone-target interactions

doi:10.1083/jcb.121.6.1369

This Article

	Full Text (PDF, 5269K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Lin, C. H.
	Articles by Forscher, P.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Lin, C. H.
	Articles by Forscher, P.


Social Bookmarking

	What's this?

ARTICLES

Cytoskeletal remodeling during growth cone-target interactions

CH Lin and P Forscher
Department of Biology, Yale University, New Haven, Connecticut 06511.

Reorganization of the cytoskeleton of neuronal growth cones in response to environmental cues underlies the process of axonal guidance. Most previous studies addressing cytoskeletal changes during growth cone pathfinding have focused on the dynamics of a single cytoskeletal component. We report here an investigation of homophilic growth cone- target interactions between Aplysia bag cell neurons using digitally enhanced video microscopy, which addresses dynamic interactions between actin filaments and microtubules. After physical contact of a growth cone with a physiological target, mechanical coupling occurred after a delay; and then the growth cone exerted forces on and displaced the target object. Subsequent to coupling, F-actin accumulation was observed at the target contact zone, followed by preferential microtubule extension to the same site. After successful target interactions, growth cones typically moved off highly adhesive poly-L- lysine substrates into native target cell surfaces. These events were associated with modulation of both the direction and rate of neurite outgrowth: growth cone migration was typically reoriented to a trajectory along the target interaction axis and rates of advance increased by about one order of magnitude. Directed microtubule movements toward the contact site appeared to be F-actin dependent as target site-specific microtubule extension and bundling could be reversibly randomized by micromolar levels of cytochalasin B in a characteristic manner. Our results suggest that target contacts can induce focal F-actin assembly and reorganization which, in turn, guides target site-directed microtubule redistribution.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Fuentes, F., Arregui, C. O. (2009). Microtubule and Cell Contact Dependency of ER-bound PTP1B Localization in Growth Cones. Mol. Biol. Cell 20: 1878-1889 [Abstract] [Full Text]
Zhang, Y., Helm, J. S., Senatore, A., Spafford, J. D., Kaczmarek, L. K., Jonas, E. A. (2008). PKC-Induced Intracellular Trafficking of CaV2 Precedes Its Rapid Recruitment to the Plasma Membrane. J. Neurosci. 28: 2601-2612 [Abstract] [Full Text]
Mimura, F., Yamagishi, S., Arimura, N., Fujitani, M., Kubo, T., Kaibuchi, K., Yamashita, T. (2006). Myelin-associated Glycoprotein Inhibits Microtubule Assembly by a Rho-kinase-dependent Mechanism. J. Biol. Chem. 281: 15970-15979 [Abstract] [Full Text]
Myers, K. A., He, Y., Hasaka, T. P., Baas, P. W. (2006). Microtubule Transport in the Axon: Re-thinking a Potential Role for the Actin Cytoskeleton. Neuroscientist 12: 107-118 [Abstract]
Alberts, P., Rudge, R., Irinopoulou, T., Danglot, L., Gauthier-Rouviere, C., Galli, T. (2006). Cdc42 and Actin Control Polarized Expression of TI-VAMP Vesicles to Neuronal Growth Cones and Their Fusion with the Plasma Membrane. Mol. Biol. Cell 17: 1194-1203 [Abstract] [Full Text]
Lehmann, M. J., Sherer, N. M., Marks, C. B., Pypaert, M., Mothes, W. (2005). Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. JCB 170: 317-325 [Abstract] [Full Text]
Bouquet, C., Soares, S., von Boxberg, Y., Ravaille-Veron, M., Propst, F., Nothias, F. (2004). Microtubule-Associated Protein 1B Controls Directionality of Growth Cone Migration and Axonal Branching in Regeneration of Adult Dorsal Root Ganglia Neurons. J. Neurosci. 24: 7204-7213 [Abstract] [Full Text]
Dent, E. W., Tang, F., Kalil, K. (2003). Axon Guidance by Growth Cones and Branches: Common Cytoskeletal and Signaling Mechanisms. Neuroscientist 9: 343-353 [Abstract]
Hussain, N. K., Yamabhai, M., Bhakar, A. L., Metzler, M., Ferguson, S. S. G., Hayden, M. R., McPherson, P. S., Kay, B. K. (2003). A Role for Epsin N-terminal Homology/AP180 N-terminal Homology (ENTH/ANTH) Domains in Tubulin Binding. J. Biol. Chem. 278: 28823-28830 [Abstract] [Full Text]
Sepp, K. J., Auld, V. J. (2003). RhoA and Rac1 GTPases mediate the dynamic rearrangement of actin in peripheral glia. Development 130: 1825-1835 [Abstract] [Full Text]
Schaefer, A. W., 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. JCB 158: 139-152 [Abstract] [Full Text]
Zhou, F.-Q., Waterman-Storer, C. M., Cohan, C. S. (2002). Focal loss of actin bundles causes microtubule redistribution and growth cone turning. JCB 157: 839-849 [Abstract] [Full Text]
Lee, S., Kolodziej, P. A. (2002). Short Stop provides an essential link between F-actin and microtubules during axon extension. Development 129: 1195-1204 [Abstract] [Full Text]
Dent, E. W., Kalil, K. (2001). Axon Branching Requires Interactions between Dynamic Microtubules and Actin Filaments. J. Neurosci. 21: 9757-9769 [Abstract] [Full Text]
Suter, D. M., Forscher, P. (2001). Transmission of growth cone traction force through apCAM-cytoskeletal linkages is regulated by Src family tyrosine kinase activity. JCB 155: 427-438 [Abstract] [Full Text]
Zhou, F.-q., Cohan, C. S. (2001). Growth Cone Collapse through Coincident Loss of Actin Bundles and Leading Edge Actin without Actin Depolymerization. JCB 153: 1071-1084 [Abstract] [Full Text]
Yvon, A.-M. C., Wadsworth, P. (2000). Region-Specific Microtubule Transport in Motile Cells. JCB 151: 1003-1012 [Abstract] [Full Text]
Matus, A. (2000). Actin-Based Plasticity in Dendritic Spines. Science 290: 754-758 [Abstract] [Full Text]
Meberg, P. J., Bamburg, J. R. (2000). Increase in Neurite Outgrowth Mediated by Overexpression of Actin Depolymerizing Factor. J. Neurosci. 20: 2459-2469 [Abstract] [Full Text]
Lautermilch, N. J., Spitzer, N. C. (2000). Regulation of Calcineurin by Growth Cone Calcium Waves Controls Neurite Extension. J. Neurosci. 20: 315-325 [Abstract] [Full Text]
Henson, J. H., Svitkina, T. M., Burns, A. R., Hughes, H. E., MacPartland, K. J., Nazarian, R., Borisy, G. G. (1999). Two Components of Actin-based Retrograde Flow in Sea Urchin Coelomocytes. Mol. Biol. Cell 10: 4075-4090 [Abstract] [Full Text]
Dent, E. W., Callaway, J. L., Szebenyi, G., Baas, P. W., Kalil, K. (1999). Reorganization and Movement of Microtubules in Axonal Growth Cones and Developing Interstitial Branches. J. Neurosci. 19: 8894-8908 [Abstract] [Full Text]
Murray, M. J., Whitington, P. M. (1999). Effects of roundabout on Growth Cone Dynamics, Filopodial Length, and Growth Cone Morphology at the Midline and throughout the Neuropile. J. Neurosci. 19: 7901-7912 [Abstract] [Full Text]
Katoh, K., Hammar, K., Smith, P. J. S., Oldenbourg, R. (1999). Arrangement of radial actin bundles in the growth cone of Aplysia bag cell neurons shows the immediate past history of filopodial behavior. Proc. Natl. Acad. Sci. USA 96: 7928-7931 [Abstract] [Full Text]
Rochlin, M. W., Dailey, M. E., Bridgman, P. C. (1999). Polymerizing Microtubules Activate Site-directed F-Actin Assembly in Nerve Growth Cones. Mol. Biol. Cell 10: 2309-2327 [Abstract] [Full Text]
Lau, P.-m., Zucker, R. S., Bentley, D. (1999). Induction of Filopodia by Direct Local Elevation of Intracellular Calcium Ion Concentration. JCB 145: 1265-1276 [Abstract] [Full Text]
Burden-Gulley, S. M., Brady-Kalnay, S. M. (1999). PTP{micro} Regulates N-Cadherin-dependent Neurite Outgrowth. JCB 144: 1323-1336 [Abstract] [Full Text]
Nabi, I. (1999). The polarization of the motile cell. J. Cell Sci. 112: 1803-1811 [Abstract]
Sider, J., Mandato, C., Weber, K., Zandy, A., Beach, D, Finst, R., Skoble, J, Bement, W. (1999). Direct observation of microtubule-f-actin interaction in cell free lysates. J. Cell Sci. 112: 1947-1956 [Abstract]
Katoh, K., Hammar, K., Smith, P. J.�S., Oldenbourg, R. (1999). Birefringence Imaging Directly Reveals Architectural Dynamics of Filamentous Actin in Living Growth Cones. Mol. Biol. Cell 10: 197-210 [Abstract] [Full Text]
Suter, D. M., Errante, L. D., Belotserkovsky, V., Forscher, P. (1998). The Ig Superfamily Cell Adhesion Molecule, apCAM, Mediates Growth Cone Steering by Substrate-Cytoskeletal Coupling. JCB 141: 227-240 [Abstract] [Full Text]
Ziv, N. E., Spira, M. E. (1998). Induction of Growth Cone Formation by Transient and Localized Increases of Intracellular Proteolytic Activity. JCB 140: 223-232 [Abstract] [Full Text]
Kaufmann, N, Wills, Z., Van Vactor, D (1998). Drosophila Rac1 controls motor axon guidance. Development 125: 453-461 [Abstract]
He, Q., Dent, E. W., Meiri, K. F. (1997). Modulation of Actin Filament Behavior by GAP-43 (Neuromodulin) Is Dependent on the Phosphorylation Status of Serine 41,�the Protein Kinase C Site. J. Neurosci. 17: 3515-3524 [Abstract] [Full Text]
Ziv, N. E., Spira, M. E. (1997). Localized and Transient Elevations of Intracellular Ca2+ Induce the Dedifferentiation of Axonal Segments into Growth Cones. J. Neurosci. 17: 3568-3579 [Abstract] [Full Text]
Challacombe, J. F., Snow, D. M., Letourneau, P. C. (1997). Dynamic Microtubule Ends Are Required for Growth Cone Turning to Avoid an Inhibitory Guidance Cue. J. Neurosci. 17: 3085-3095 [Abstract] [Full Text]
Cunningham, C. C., Leclerc, N., Flanagan, L. A., Lu, M., Janmey, P. A., Kosik, K. S. (1997). Microtubule-associated Protein 2c Reorganizes Both Microtubules and Microfilaments into Distinct Cytological Structures in an Actin-binding Protein-280-deficient Melanoma Cell Line. JCB 136: 845-857 [Abstract] [Full Text]
Mason, C. A., Wang, L.-C. (1997). Growth Cone Form Is Behavior-Specific and, Consequently, Position-Specific along the Retinal Axon Pathway. J. Neurosci. 17: 1086-1100 [Abstract] [Full Text]
Rajnicek, A, McCaig, C (1997). Guidance of CNS growth cones by substratum grooves and ridges: effects of inhibitors of the cytoskeleton, calcium channels and signal transduction pathways. J. Cell Sci. 110: 2915-2924 [Abstract]
Williamson, T., Gordon-Weeks, P.�R., Schachner, M., Taylor, J. (1996). Microtubule reorganization is obligatory for growth cone�turning. Proc. Natl. Acad. Sci. USA 93: 15221-15226 [Abstract] [Full Text]
Rochlin, M. W., Wickline, K. M., Bridgman, P. C. (1996). Microtubule Stability Decreases Axon Elongation but Not Axoplasm Production. J. Neurosci. 16: 3236-3246 [Abstract] [Full Text]
Thompson, C, Lin, C., Forscher, P (1996). An Aplysia cell adhesion molecule associated with site-directed actin filament assembly in neuronal growth cones. J. Cell Sci. 109: 2843-2854 [Abstract]
Challacombe, J., Snow, D., Letourneau, P. (1996). Actin filament bundles are required for microtubule reorientation during growth cone turning to avoid an inhibitory guidance cue. J. Cell Sci. 109: 2031-2040 [Abstract]
Zachow, K., Bentley, D (1996). Blackjack, a novel protein associated with microtubules in embryonic neurons. J. Cell Sci. 109: 1497-1507 [Abstract]
Kapeller, R., Toker, A., Cantley, L. C., Carpenter, C. L. (1995). Phosphoinositide 3-Kinase Binds Constitutively to alpha/beta-Tubulin and Binds to [IMAGE]-Tubulin in Response to Insulin. J. Biol. Chem. 270: 25985-25991 [Abstract] [Full Text]