Involvement of microtubules in the regulation of neuronal growth cone morphologic remodeling

Gallo, Gianluca

doi:10.1002/(sici)1097-4695(199805)35:2<121::aid-neu1>3.0.co;2-6

Cited by 27 publications

(16 citation statements)

References 68 publications

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“…Consistent with these findings, pharmacological inhibition of microtubule dynamics in growth cones decreases the extent of lamellipodial protrusion (Gallo, 1998). Interestingly, the depolymerization of microtubules from growth cones can also result in the transient hyperextension of growth cone lamellipodia and filopodia (Gallo, 1998), suggesting that microtubules may also be part of the mechanism that limits protrusive activity to the ends of axons (Bray et al, 1978). Similar transient overproduction of lamellipodia has been observed in studies of the effects of microtubule depolymerization in nonneuronal cells (Rosania and Swanson, 1996;Mikhailov and Gundersen, 1998), and these results have been interpreted as indicating that dynamic microtubules act as delivery systems for molecules that regulate lamellipodial behavior and that become released upon microtubule depolymerization.…”

Section: Protrusionsupporting

confidence: 72%

“…The importance of microtubule dynamics in axon elongation is underscored by the fact that inhibition of microtubule dynamic instability reduces the rate of axon elongation Rochlin et al, 1996;Challacombe et al, 1997;Gallo, 1998;Gallo and Letourneau, 1999). A role for dynamic microtubule tips in the engorgement phase of axonal elongation is also supported by the observations that inhibition of microtubule dynamic instability prevents the movement of organelles from the C-into the P-domain (Gallo, 1998) and the insertion of membrane into the growth cone plasmalemma (Zakharenko and Popov, 1998).…”

Section: Engorgementmentioning

confidence: 99%

“…Time-lapse observations of fluorescently labeled microtubules in living growth cones have determined that the tips of axonal microtubules continuously probe the P-domain Kirschner, 1991, 1995). These microtubule tips invade the P-domain in a manner mostly dependent on microtubule dynamic instability, as demonstrated by studies with pharmacological inhibitors of dynamic instability Rochlin et al, 1996;Challacombe et al, 1997;Gallo, 1998). The importance of microtubule dynamics in axon elongation is underscored by the fact that inhibition of microtubule dynamic instability reduces the rate of axon elongation Rochlin et al, 1996;Challacombe et al, 1997;Gallo, 1998;Gallo and Letourneau, 1999).…”

Section: Engorgementmentioning

confidence: 99%

“…However, neurotrophins have been implicated in the regulation of axonal branch arborization within target tissues (McAllister et al, 1999). To study the cellular mechanisms of neurotrophin regulation of the neuronal cytoskeleton, we have developed an in vitro model system for the localized presentation of neurotrophins to axons and growth cones (Gallo andLetourneau, 1997, 1998). In short, neurotrophins are covalently bound to polystyrene beads, and the responses to contact with neurotrophin-coated beads by growth cones are monitored with time-lapse video-microscopy and immunocytochemical staining for F-actin and microtubules.…”

Section: Neurotrophin-mediated Regulation Of Neuronal Motility and Thmentioning

confidence: 99%

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Neurotrophins and the dynamic regulation of the neuronal cytoskeleton

Gallo

Letourneau

2000

J. Neurobiol.

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The morphology of neuronal axons and dendrites is dependent on the dynamics of the cytoskeleton. An understanding of neurodevelopment and adult neuroplasticity must therefore include a detailed description of the intrinsic and extrinsic mechanisms that regulate the organization and dynamics of actin filaments and microtubules. In this paper we review recent advances in the understanding of the dynamic regulation of neuronal morphology by interactions among cytoskeletal components and the regulation of the cytoskeleton by neurotrophins.

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Section: Protrusionsupporting

confidence: 72%

Section: Engorgementmentioning

confidence: 99%

Section: Engorgementmentioning

confidence: 99%

Section: Neurotrophin-mediated Regulation Of Neuronal Motility and Thmentioning

confidence: 99%

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Neurotrophins and the dynamic regulation of the neuronal cytoskeleton

Gallo

Letourneau

2000

J. Neurobiol.

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“…Similar to f-actin, the role of microtubules for neuron growth has been well documented (Gallo 1998;Dehmelt and Halpain 2004;Gordon-Weeks 2004). We used a fluorescent conjugate of paclitaxel in order to investigate the distribution of microtubules within the optic nerve of developing stalk-eyed flies.…”

Section: The Gross Morphological Distribution Of Tubulinmentioning

confidence: 94%

The development of a long, coiled, optic nerve in the stalk-eyed fly Cyrtodiopsis whitei

Buschbeck

Hoy

2005

Cell Tissue Res

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In the stalk-eyed fly Cyrtodiopsis whitei (Diopsidae; Diptera), the relatively long optic nerve develops within the tight lumen of a very short eyestalk. Axonal growth is generally considered in terms of path finding, selective fasciculation, and towing. Physical forces that are necessary for axon lengthening are generated either by the growth cone or by the growth of surrounding tissues. Therefore, it is surprising to encounter a loosely coiled nerve apparently lacking any attachments that could allow for pull, or towing, of the nerve. In this study, we used histological sections and whole-mount preparations to confirm that the optic nerve of the stalk-eyed fly indeed elongates without the external application of tension to the nerve. Secondly, we examined the distribution of cytoskeletal elements and selected proteins that may be involved in axon extension. Staining against the vesicle fusion proteins SNAP-24 and SNAP-25 consistently results in stronger staining in the rapidly extending optic nerve than in a control nerve, suggesting a possible role of these proteins in the extension process. On a gross morphological level, SNAP-24/25 as well as the cytoskeletal elements actin and tubulin are uniformly distributed throughout the lengths of the growing nerve, suggesting that nerve elongation is distributed rather than localized. Finally, we identified glia as a possible source for tension within the nerve bundle. Glia proliferate rapidly in the optic nerve but not in the control nerve. Much work continues to focus on the growth of axons in culture, but this study is one of the few that considers the dynamics of nerve bundle extension as a whole.

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Identification and characterization of a population of motile neurons in long‐term cortical culture

Haas

Chuckowree

Chung

et al. 2007

Cell Motil. Cytoskeleton

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The specific phenotypes and progression to maturity of primary cortical neurons in long-term culture correlate well with neurons in vivo. Utilizing a model of neuronal injury in long-term cultures at 21 days in vitro (DIV), we have identified a distinct population of neurons that translocate into the injury site. 5-bromo-2'-deoxyUridine (BrdU) incorporation studies demonstrated that neurons with the capacity to translocate were 21 days old. However, this motile ability is not consistent with the traditional view of the maturation and structural stability of neurons in long-term culture. Therefore, we examined the neurons' cytoskeletal profile using immunocytochemistry, to establish relative stage of maturation and phenotype. Expression of marker proteins including beta-III-tubulin, alpha-internexin, NF-L and NF-M, tau and L1 indicated the neurons were differentiated, and in some cases polarized. The neurons did not immunolabel with NF-H or MAP2, which might suggest they had not reached the level of maturity of other neurons in culture. They did not express the microtubule-associated migration marker doublecortin (DCX). Cytoskeletal disrupting agents were used to further investigate the role of the microtubule cytoskeleton in translocation, and microtubule destabilization significantly enhanced aspects of their motility. Finally, molecular guidance cues affected their motility in a similar manner to that reported for both axon guidance and early neuron migration. Therefore, this study has identified and characterized a population of motile neurons in vitro that have the capacity to migrate into a site of injury. These studies provide new information on the structurally dynamic features of subsets of neurons.

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Involvement of microtubules in the regulation of neuronal growth cone morphologic remodeling

Cited by 27 publications

References 68 publications

Neurotrophins and the dynamic regulation of the neuronal cytoskeleton

Neurotrophins and the dynamic regulation of the neuronal cytoskeleton

The development of a long, coiled, optic nerve in the stalk-eyed fly Cyrtodiopsis whitei

Identification and characterization of a population of motile neurons in long‐term cortical culture

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