Hierarchical microtubule organization controls axon caliber and transport and determines synaptic structure and stability

Raiko Stephan; Bernd Goellner; Eliza Moreno; C Andrew Frank; Tabea Hugenschmidt; Christel Genoud; Hermann Aberle; Jan Pielage

doi:10.1016/j.devcel.2015.02.003

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Hierarchical microtubule organization controls axon caliber and transport and determines synaptic structure and stability

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Hierarchical microtubule organization controls axon caliber and transport and determines synaptic structure and stability

Raiko Stephan, Bernd Goellner, Eliza Moreno, C Andrew Frank, Tabea Hugenschmidt, Christel Genoud, Hermann Aberle and Jan Pielage

Developmental cell, Vol.33(1), pp.5-21

04/06/2015

DOI: 10.1016/j.devcel.2015.02.003

PMCID: PMC5906805

PMID: 25800091

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Abstract

The dimensions of axons and synaptic terminals determine cell-intrinsic properties of neurons; however, the cellular mechanisms selectively controlling establishment and maintenance of neuronal compartments remain poorly understood. Here, we show that two giant Drosophila Ankyrin2 isoforms, Ank2-L and Ank2-XL, and the MAP1B homolog Futsch form a membrane-associated microtubule-organizing complex that determines axonal diameter, supports axonal transport, and provides independent control of synaptic dimensions and stability. Ank2-L controls microtubule and synaptic stability upstream of Ank2-XL that selectively controls microtubule organization. Synergistically with Futsch, Ank2-XL provides three-dimensional microtubule organization and is required to establish appropriate synaptic dimensions and release properties. In axons, the Ank2-XL/Futsch complex establishes evenly spaced, grid-like microtubule organization and determines axonal diameter in the absence of neurofilaments. Reduced microtubule spacing limits anterograde transport velocities of mitochondria and synaptic vesicles. Our data identify control of microtubule architecture as a central mechanism to selectively control neuronal dimensions, functional properties, and connectivity.

Microtubule-Associated Proteins - metabolism

Neuromuscular Junction - metabolism

Synapses - physiology

Electrophysiology

Axonal Transport - physiology

Neurons - cytology

Drosophila Proteins - metabolism

Animals, Genetically Modified - metabolism

Drosophila melanogaster - genetics

Immunoenzyme Techniques

Drosophila melanogaster - metabolism

Microtubules - metabolism

Animals

Image Processing, Computer-Assisted

Animals, Genetically Modified - genetics

Ankyrins - metabolism

Cytoskeleton - metabolism

Neurons - metabolism

Details

Title: Subtitle: Hierarchical microtubule organization controls axon caliber and transport and determines synaptic structure and stability
Creators: Raiko Stephan - Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland
Bernd Goellner - Heinrich-Heine-University Düsseldorf, Universitätsstrasse 1, 40225 Düsseldorf, Germany
Eliza Moreno - Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland
C Andrew Frank - Department of Anatomy and Cell Biology, University of Iowa, 51 Newton Road, Iowa City, IA 52242, USA
Tabea Hugenschmidt - Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland
Christel Genoud - Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland
Hermann Aberle - Heinrich-Heine-University Düsseldorf, Universitätsstrasse 1, 40225 Düsseldorf, Germany
Jan Pielage - Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland. Electronic address: jan.pielage@fmi.ch
Resource Type: Journal article
Publication Details: Developmental cell, Vol.33(1), pp.5-21
Publisher: United States
DOI: 10.1016/j.devcel.2015.02.003
PMID: 25800091
PMCID: PMC5906805
ISSN: 1534-5807
eISSN: 1878-1551
Grant note: R00 NS062738 / NINDS NIH HHS
Language: English
Date published: 04/06/2015
Academic Unit: Anatomy and Cell Biology; Iowa Neuroscience Institute
Record Identifier: 9984025447402771

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