Microtubule behavior during guidance of pioneer neuron growth cones in situ

doi:10.1083/jcb.115.2.381

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Microtubule behavior during guidance of pioneer neuron growth cones in situ

JH Sabry, TP O'Connor, L Evans, A Toroian-Raymond, M Kirschner and D Bentley
Department of Biochemistry and Biophysics, University of California, San Francisco 94143.

The growth of an axon toward its target results from the reorganization of the cytoskeleton in response to environmental guidance cues. Recently developed imaging technology makes it possible to address the effect of such cues on the neural cytoskeleton directly. Although high resolution studies can be carried out on neurons in vitro, these circumstances do not recreate the complexity of the natural environment. We report here on the arrangement and dynamics of microtubules in live neurons pathfinding in response to natural guidance cues in situ using the embryonic grasshopper limb fillet preparation. A rich microtubule network was present within the body of the growth cone and normally extended into the distal growth cone margin. Complex microtubule loops often formed transiently within the growth cone. Branches both with and without microtubules were regularly observed. Microtubules did not extend into filopodia. During growth cone steering events in response to identified guidance cues, microtubule behaviour could be monitored. In turns towards guidepost cells, microtubules selectively invaded branches derived from filopodia that had contacted the guidepost cell. At limb segment boundaries, microtubules displayed a variety of behaviors, including selective branch invasion, and also invasion of multiple branches followed by selective retention in branches oriented in the correct direction. Microtubule invasion of multiple branches also was seen in growth cones migrating on intrasegmental epithelium. Both selective invasion and selective retention generate asymmetrical microtubule arrangements within the growth cone, and may play a key role in growth cone steering events.
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Geraldo, S., Gordon-Weeks, P. R. (2009). Cytoskeletal dynamics in growth-cone steering. J. Cell Sci. 122: 3595-3604 [Abstract] [Full Text]
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Hendricks, M., Jesuthasan, S. (2009). PHR Regulates Growth Cone Pausing at Intermediate Targets through Microtubule Disassembly. J. Neurosci. 29: 6593-6598 [Abstract] [Full Text]
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]
Erturk, A., Hellal, F., Enes, J., Bradke, F. (2007). Disorganized Microtubules Underlie the Formation of Retraction Bulbs and the Failure of Axonal Regeneration. J. Neurosci. 27: 9169-9180 [Abstract] [Full Text]
Dwivedy, A., Gertler, F. B., Miller, J., Holt, C. E., Lebrand, C. (2007). Ena/VASP function in retinal axons is required for terminal arborization but not pathway navigation. Development 134: 2137-2146 [Abstract] [Full Text]
Lee, S., Nahm, M., Lee, M., Kwon, M., Kim, E., Zadeh, A. D., Cao, H., Kim, H.-J., Lee, Z. H., Oh, S. B., Yim, J., Kolodziej, P. A., Lee, S. (2007). The F-actin-microtubule crosslinker Shot is a platform for Krasavietz-mediated translational regulation of midline axon repulsion. Development 134: 1767-1777 [Abstract] [Full Text]
Lovell, P., Moroz, L. L. (2006). The largest growth cones in the animal kingdom: an illustrated guide to the dynamics of Aplysia neuronal growth in cell culture. Integr. Comp. Biol. 46: 847-870 [Abstract] [Full Text]
Brown, H. L. D., Cherbas, L., Cherbas, P., Truman, J. W. (2006). Use of time-lapse imaging and dominant negative receptors to dissect the steroid receptor control of neuronal remodeling in Drosophila. Development 133: 275-285 [Abstract] [Full Text]
Arimura, N., Menager, C., Kawano, Y., Yoshimura, T., Kawabata, S., Hattori, A., Fukata, Y., Amano, M., Goshima, Y., Inagaki, M., Morone, N., Usukura, J., Kaibuchi, K. (2005). Phosphorylation by Rho Kinase Regulates CRMP-2 Activity in Growth Cones. Mol. Cell. Biol. 25: 9973-9984 [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]
Legg, A. T., O'Connor, T. P. (2003). Gradients and Growth Cone Guidance of Grasshopper Neurons. J. Histochem. Cytochem. 51: 445-454 [Abstract] [Full Text]
Tang, F., Dent, E. W., Kalil, K. (2003). Spontaneous Calcium Transients in Developing Cortical Neurons Regulate Axon Outgrowth. J. Neurosci. 23: 927-936 [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]
Noiges, R., Eichinger, R., Kutschera, W., Fischer, I., Nemeth, Z., Wiche, G., Propst, F. (2002). Microtubule-Associated Protein 1A (MAP1A) and MAP1B: Light Chains Determine Distinct Functional Properties. J. Neurosci. 22: 2106-2114 [Abstract] [Full Text]
Kim, M. D., Kolodziej, P., Chiba, A. (2002). Growth Cone Pathfinding and Filopodial Dynamics Are Mediated Separately by Cdc42 Activation. J. Neurosci. 22: 1794-1806 [Abstract] [Full Text]
Scott, G., Leopardi, S., Printup, S., Madden, B. C. (2002). Filopodia are conduits for melanosome transfer to keratinocytes. J. Cell Sci. 115: 1441-1451 [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]
Zmuda, J., Rivas, R. (2000). Actin disruption alters the localization of tau in the growth cones of cerebellar granule neurons. J. Cell Sci. 113: 2797-2809 [Abstract]
Takei, K., Chan, T. A., Wang, F.-S., Deng, H., Rutishauser, U., Jay, D. G. (1999). The Neural Cell Adhesion Molecules L1 and NCAM-180 Act in Different Steps of Neurite Outgrowth. J. Neurosci. 19: 9469-9479 [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]
Mallavarapu, A., Mitchison, T. (1999). Regulated Actin Cytoskeleton Assembly at Filopodium Tips Controls Their Extension and Retraction. JCB 146: 1097-1106 [Abstract] [Full Text]
Isbister, C. M., O'Connor, T. P. (1999). Filopodial Adhesion Does Not Predict Growth Cone Steering Events In Vivo. J. Neurosci. 19: 2589-2600 [Abstract] [Full Text]
Togel, M., Wiche, G., Propst, F. (1998). Novel Features of the Light Chain of Microtubule-associated Protein MAP1B: Microtubule Stabilization, Self Interaction, Actin Filament Binding, and Regulation by the Heavy Chain. JCB 143: 695-707 [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]
Antonsson, B., Kassel, D. B., Di Paolo, G., Lutjens, R., Riederer, B. M., Grenningloh, G. (1998). Identification of in Vitro Phosphorylation Sites in the Growth Cone Protein SCG10. EFFECT OF PHOSPHORYLATION SITE MUTANTS ON MICROTUBULE-DESTABILIZING ACTIVITY. J. Biol. Chem. 273: 8439-8446 [Abstract] [Full Text]
Beinhauer, J. D., Hagan, I. M., Hegemann, J. H., Fleig, U. (1997). Mal3, the Fission Yeast Homologue of the Human APC-interacting Protein EB-1 Is Required for Microtubule Integrity and the Maintenance of Cell Form. JCB 139: 717-728 [Abstract] [Full Text]
Pollack, A. L., Barth, A. I.M., Altschuler, Y., Nelson, W. J., Mostov, K. E. (1997). Dynamics of {beta}-Catenin Interactions with APC Protein Regulate Epithelial Tubulogenesis. JCB 137: 1651-1662 [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]
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]
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]
Estes, P. S., Roos, J., van der Bliek, A., Kelly, R. B., Krishnan, K. S., Ramaswami, M. (1996). Traffic of Dynamin within Individual Drosophila Synaptic Boutons Relative to Compartment-Specific Markers. J. Neurosci. 16: 5443-5456 [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]
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]
Ueda, M, Ogihara, S (1994). Microtubules are required in amoeba chemotaxis for preferential stabilization of appropriate pseudopods. J. Cell Sci. 107: 2071-2079 [Abstract]
Paturle-Lafanechere, L, Manier, M, Trigault, N, Pirollet, F, Mazarguil, H, Job, D (1994). Accumulation of delta 2-tubulin, a major tubulin variant that cannot be tyrosinated, in neuronal tissues and in stable microtubule assemblies. J. Cell Sci. 107: 1529-1543 [Abstract]
Esmaeli-Azad, B, McCarty, J., Feinstein, S. (1994). Sense and antisense transfection analysis of tau function: tau influences net microtubule assembly, neurite outgrowth and neuritic stability. J. Cell Sci. 107: 869-879 [Abstract]
Zheng, J, Buxbaum, R., Heidemann, S. (1993). Investigation of microtubule assembly and organization accompanying tension-induced neurite initiation. J. Cell Sci. 104: 1239-1250 [Abstract]
Brown, A, Li, Y, Slaughter, T, Black, M. (1993). Composite microtubules of the axon: quantitative analysis of tyrosinated and acetylated tubulin along individual axonal microtubules. J. Cell Sci. 104: 339-352 [Abstract]