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Polarized microtubule arrays in apical dendrites and axons.

ABSTRACT: The polarization of microtubules within neurons in vivo is crucial in their role of determining the directions and speeds of intracellular transport. More than a decade ago, electron microscopy studies of mature hippocampal cultures indicated that their axons contained microtubules of uniform polarity and that dendrites contained microtubules of mixed polarity. Here, we evaluated polarity distributions in native brain tissues and in cultures by using multiphoton microscopy and second-harmonic generation from microtubules. We confirmed the expected polarized microtubule arrays in axons; however, we also unexpectedly found them ubiquitously in apical dendrites of mature hippocampal CA1 and cortical layer V pyramidal neurons. Some of these organized dendritic microtubule arrays extended for >270 microm with overall polarity of >80%. Our research indicates neurite-specific and age-dependent microtubule organizations that have direct implications for neuronal cargo transport.

SUBMITTER: Kwan AC

PROVIDER: S-EPMC2496886 | biostudies-literature | 2008 Aug

REPOSITORIES: biostudies-literature

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Polarized microtubule arrays in apical dendrites and axons.

Kwan Alex C AC Dombeck Daniel A DA Webb Watt W WW

Proceedings of the National Academy of Sciences of the United States of America 20080805 32

The polarization of microtubules within neurons in vivo is crucial in their role of determining the directions and speeds of intracellular transport. More than a decade ago, electron microscopy studies of mature hippocampal cultures indicated that their axons contained microtubules of uniform polarity and that dendrites contained microtubules of mixed polarity. Here, we evaluated polarity distributions in native brain tissues and in cultures by using multiphoton microscopy and second-harmonic ge ...[more]

PMID: 18682556

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Project description:BackgroundDendrites differ from axons in patterns of growth and development, as well as in morphology. Given that microtubules are key structural elements in cells, we assessed patterns of microtubule stability and polymerization during hippocampal neuron development in vitro to determine if these aspects of microtubule organization could distinguish axons from dendrites.ResultsQuantitative ratiometric immunocytochemistry identified significant differences in microtubule stability between axons and dendrites. Most notably, regardless of developmental stage, there were high levels of dynamic microtubules throughout the dendritic arbor, whereas dynamic microtubules were predominantly concentrated in the distal end of axons. Analysis of microtubule polymerization using green fluorescent protein-tagged EB1 showed both developmental and regional differences in microtubule polymerization between axons and dendrites. Early in development (for example, 1 to 2 days in vitro), polymerization events were distributed equally in both the anterograde and retrograde directions throughout the length of both axons and dendrites. As development progressed, however, polymerization became biased, with a greater number of polymerization events in distal than in proximal and middle regions. While polymerization occurred almost exclusively in the anterograde direction for axons, both anterograde and retrograde polymerization was observed in dendrites. This is in agreement with predicted differences in microtubule polarity within these compartments, although fewer retrograde events were observed in dendrites than expected.ConclusionBoth immunocytochemical and live imaging analyses showed that newly formed microtubules predominated at the distal end of axons and dendrites, suggesting a common mechanism that incorporates increased microtubule polymerization at growing process tips. Dendrites had more immature, dynamic microtubules throughout the entire arbor than did axons, however. Identifying these differences in microtubule stability and polymerization is a necessary first step toward understanding how they are developmentally regulated, and may reveal novel mechanisms underlying neuron maturation and dendritic plasticity that extend beyond the initial specification of polarity.

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Polarized microtubule arrays in apical dendrites and axons.

Publications

Polarized microtubule arrays in apical dendrites and axons.

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