Literature DB >> 27162329

Prevalent presence of periodic actin-spectrin-based membrane skeleton in a broad range of neuronal cell types and animal species.

Jiang He1, Ruobo Zhou1, Zhuhao Wu2, Monica A Carrasco3, Peri T Kurshan4, Jonathan E Farley5, David J Simon2, Guiping Wang1, Boran Han1, Junjie Hao1, Evan Heller1, Marc R Freeman5, Kang Shen4, Tom Maniatis3, Marc Tessier-Lavigne2, Xiaowei Zhuang6.   

Abstract

Actin, spectrin, and associated molecules form a periodic, submembrane cytoskeleton in the axons of neurons. For a better understanding of this membrane-associated periodic skeleton (MPS), it is important to address how prevalent this structure is in different neuronal types, different subcellular compartments, and across different animal species. Here, we investigated the organization of spectrin in a variety of neuronal- and glial-cell types. We observed the presence of MPS in all of the tested neuronal types cultured from mouse central and peripheral nervous systems, including excitatory and inhibitory neurons from several brain regions, as well as sensory and motor neurons. Quantitative analyses show that MPS is preferentially formed in axons in all neuronal types tested here: Spectrin shows a long-range, periodic distribution throughout all axons but appears periodic only in a small fraction of dendrites, typically in the form of isolated patches in subregions of these dendrites. As in dendrites, we also observed patches of periodic spectrin structures in a small fraction of glial-cell processes in four types of glial cells cultured from rodent tissues. Interestingly, despite its strong presence in the axonal shaft, MPS is disrupted in most presynaptic boutons but is present in an appreciable fraction of dendritic spine necks, including some projecting from dendrites where such a periodic structure is not observed in the shaft. Finally, we found that spectrin is capable of adopting a similar periodic organization in neurons of a variety of animal species, including Caenorhabditis elegans, Drosophila, Gallus gallus, Mus musculus, and Homo sapiens.

Entities:  

Keywords:  STORM; actin; cytoskeleton; neuron; spectrin

Mesh:

Substances:

Year:  2016        PMID: 27162329      PMCID: PMC4889411          DOI: 10.1073/pnas.1605707113

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  39 in total

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Authors:  V Bennett; A J Baines
Journal:  Physiol Rev       Date:  2001-07       Impact factor: 37.312

2.  Nanoscale Architecture of the Axon Initial Segment Reveals an Organized and Robust Scaffold.

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Journal:  Cell Rep       Date:  2015-12-17       Impact factor: 9.423

3.  Calbindin-D28k is a more reliable marker of human Purkinje cells than standard Nissl stains: a stereological experiment.

Authors:  Elizabeth R Whitney; Thomas L Kemper; Douglas L Rosene; Margaret L Bauman; Gene J Blatt
Journal:  J Neurosci Methods       Date:  2007-09-16       Impact factor: 2.390

4.  Spectrin- and ankyrin-based membrane domains and the evolution of vertebrates.

Authors:  Vann Bennett; Damaris N Lorenzo
Journal:  Curr Top Membr       Date:  2013       Impact factor: 3.049

5.  Characterization and development of photoactivatable fluorescent proteins for single-molecule-based superresolution imaging.

Authors:  Siyuan Wang; Jeffrey R Moffitt; Graham T Dempsey; X Sunney Xie; Xiaowei Zhuang
Journal:  Proc Natl Acad Sci U S A       Date:  2014-05-27       Impact factor: 11.205

6.  Cell organization, growth, and neural and cardiac development require αII-spectrin.

Authors:  Michael C Stankewich; Carol D Cianci; Paul R Stabach; Lan Ji; Anjali Nath; Jon S Morrow
Journal:  J Cell Sci       Date:  2011-12-08       Impact factor: 5.285

7.  β-III spectrin is critical for development of purkinje cell dendritic tree and spine morphogenesis.

Authors:  Yuanzheng Gao; Emma M Perkins; Yvonne L Clarkson; Steven Tobia; Alastair R Lyndon; Mandy Jackson; Jeffrey D Rothstein
Journal:  J Neurosci       Date:  2011-11-16       Impact factor: 6.167

8.  Metabotropic glutamate receptors mGluR2 and mGluR5 are expressed in two non-overlapping populations of Golgi cells in the rat cerebellum.

Authors:  A Neki; H Ohishi; T Kaneko; R Shigemoto; S Nakanishi; N Mizuno
Journal:  Neuroscience       Date:  1996-12       Impact factor: 3.590

9.  Fast, three-dimensional super-resolution imaging of live cells.

Authors:  Sara A Jones; Sang-Hee Shim; Jiang He; Xiaowei Zhuang
Journal:  Nat Methods       Date:  2011-05-08       Impact factor: 28.547

10.  Axons break in animals lacking beta-spectrin.

Authors:  Marc Hammarlund; Erik M Jorgensen; Michael J Bastiani
Journal:  J Cell Biol       Date:  2007-01-29       Impact factor: 10.539

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  59 in total

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Review 2.  Expansion microscopy: development and neuroscience applications.

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Journal:  Curr Opin Neurobiol       Date:  2018-01-06       Impact factor: 6.627

3.  A dual role for βII-spectrin in axons.

Authors:  Christophe Leterrier
Journal:  Proc Natl Acad Sci U S A       Date:  2019-07-09       Impact factor: 11.205

4.  The role of spectrin in cell adhesion and cell-cell contact.

Authors:  Beata Machnicka; Renata Grochowalska; Dżamila M Bogusławska; Aleksander F Sikorski
Journal:  Exp Biol Med (Maywood)       Date:  2019-06-21

Review 5.  The role of the membrane-associated periodic skeleton in axons.

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Journal:  Cell Mol Life Sci       Date:  2021-06-03       Impact factor: 9.261

6.  Structural organization of the actin-spectrin-based membrane skeleton in dendrites and soma of neurons.

Authors:  Boran Han; Ruobo Zhou; Chenglong Xia; Xiaowei Zhuang
Journal:  Proc Natl Acad Sci U S A       Date:  2017-07-24       Impact factor: 11.205

Review 7.  Spatial control of membrane traffic in neuronal dendrites.

Authors:  Megan R Radler; Ayana Suber; Elias T Spiliotis
Journal:  Mol Cell Neurosci       Date:  2020-04-12       Impact factor: 4.314

8.  Localized Myosin II Activity Regulates Assembly and Plasticity of the Axon Initial Segment.

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