Key Points
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Membrane for plasmalemmal expansion is generated through the secretory pathway, primarily in the neuron's perikaryon, and then transported as plasmalemmal precursor vesicles to the cell periphery for insertion. Numerous vesicle types are generated for export; they may be targeted directly to specific membrane domains or may follow a transcytotic pathway.
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Certain membrane proteins are synthesized in the axonal growth cone, but how locally synthesized membrane proteins are inserted into the plasma membrane is unknown.
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During de novo neurite outgrowth membrane insertion and expansion occur primarily at the growing tip. In synaptically connected growing neurons, however, the mechanisms and sites of membrane insertion are poorly understood.
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Exocytotic insertion of membrane vesicles at the axonal growth cone requires exocyst and SNARE proteins, and it is regulated locally.
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Dendrites receive plasmalemmal precursor vesicles from the perikaryon. In addition, they are capable of quasi-independent membrane synthesis through their own endoplasmic reticulum and Golgi outposts.
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Endocytosis and membrane recycling occur during neurite outgrowth, but net membrane retrieval and degradation seem to be minor components of membrane flux.
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Neuronal polarization, neurite outgrowth and plasmalemmal expansion are tightly linked phenomena.
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Impaired plasmalemmal expansion and maintenance might be involved in a number of neurodegenerative disorders.
Abstract
The formation of axons and dendrites and maintenance of the neuron's vastly expanded surface require the continuous addition of new membrane. This is achieved by membrane synthesis through the secretory pathway followed by regulated vesicle fusion with the plasma membrane, typically in the distal neurite. However, it is far from simple: multiple distinct membrane carriers are used to target specific membrane domains, dendrites seem to operate semi-autonomously from the rest of the neuron, and exocytosis for membrane expansion is different from that for release of synaptic vesicles. Current knowledge of this process and its implications for neuronal development, function and repair are reviewed.
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Acknowledgements
The author wishes to thank M.-F. Maylie-Pfenninger and L. Sosa for helpful discussions, and his many former and present associates for their contributions to this work. Relevant studies in the author's laboratory were supported by grants from the US National Institutes of Health and the National Science Foundation.
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Glossary
- Growth cone
-
The terminally enlarged, amoeboid tip of a neurite.
- Perikaryon
-
The portion of the neuron that surrounds the nucleus and excludes the neurites. Also referred to as the cell body.
- Microtubule plus end
-
Microtubules are polarized structures, and the plus end is the end at which polymerization predominantly occurs. By contrast, disassembly predominates at the minus end. In axons, microtubules are oriented so that the plus ends point towards the growth cone or presynaptic terminal.
- Trans-Golgi network
-
The last stage of the Golgi complex, where sorting of components and vesicle formation take place.
- Freeze fracture
-
A preparative method for electron microscopy that involves rapidly freezing and fracturing the biological sample and then shadow casting it with a metal vapour to generate a replica of the fracture face. Ultrastructural analysis of the replica reveals structures in the lipid bilayer, such as intramembrane particles, that are thought to represent membrane-protein complexes.
- Moving-boundary system
-
A system that expands with time so that diffusion in it never reaches equilibrium, as long as expansion (in this case neurite growth) exceeds the diffusion rate.
- Lectin
-
A protein that recognizes and binds to specific oligosaccharide sequences.
- Excimer
-
Very transient dimers of fluorescent molecules, one of which is in an excited state. Emission during return to the ground state is of lower energy (red shift) than that of excited monomers. The term is a contraction of 'excited dimer'.
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Pfenninger, K. Plasma membrane expansion: a neuron's Herculean task. Nat Rev Neurosci 10, 251–261 (2009). https://doi.org/10.1038/nrn2593
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DOI: https://doi.org/10.1038/nrn2593
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