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

Jiang He, Ruobo Zhou, Zhuhao Wu, Monica A. Carrasco, Peri T. Kurshan, Jonathan E. Farley, David J. Simon, Guiping Wang, Boran Han, Junjie Hao, Evan Heller, Marc R. Freeman, Kang Shen, Tom Maniatis, Marc Tessier-Lavigne, Xiaowei Zhuang

Research output: Contribution to journalArticle

60 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)6029-6034
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number21
DOIs
StatePublished - May 24 2016
Externally publishedYes

Fingerprint

Spectrin
Skeleton
Actins
Dendrites
Membranes
Neuroglia
Axons
Neurons
Dendritic Spines
Caenorhabditis elegans
Peripheral Nervous System
Motor Neurons
Sensory Receptor Cells
Cytoskeleton
Drosophila
Chickens
Rodentia
Central Nervous System
Brain

Keywords

  • Actin
  • Cytoskeleton
  • Neuron
  • Spectrin
  • STORM

ASJC Scopus subject areas

  • General

Cite this

Prevalent presence of periodic actin-spectrin-based membrane skeleton in a broad range of neuronal cell types and animal species. / He, Jiang; Zhou, Ruobo; Wu, Zhuhao; Carrasco, Monica A.; Kurshan, Peri T.; Farley, Jonathan E.; Simon, David J.; Wang, Guiping; Han, Boran; Hao, Junjie; Heller, Evan; Freeman, Marc R.; Shen, Kang; Maniatis, Tom; Tessier-Lavigne, Marc; Zhuang, Xiaowei.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, No. 21, 24.05.2016, p. 6029-6034.

Research output: Contribution to journalArticle

He, J, Zhou, R, Wu, Z, Carrasco, MA, Kurshan, PT, Farley, JE, Simon, DJ, Wang, G, Han, B, Hao, J, Heller, E, Freeman, MR, Shen, K, Maniatis, T, Tessier-Lavigne, M & Zhuang, X 2016, 'Prevalent presence of periodic actin-spectrin-based membrane skeleton in a broad range of neuronal cell types and animal species', Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 21, pp. 6029-6034. https://doi.org/10.1073/pnas.1605707113
He, Jiang ; Zhou, Ruobo ; Wu, Zhuhao ; Carrasco, Monica A. ; Kurshan, Peri T. ; Farley, Jonathan E. ; Simon, David J. ; Wang, Guiping ; Han, Boran ; Hao, Junjie ; Heller, Evan ; Freeman, Marc R. ; Shen, Kang ; Maniatis, Tom ; Tessier-Lavigne, Marc ; Zhuang, Xiaowei. / Prevalent presence of periodic actin-spectrin-based membrane skeleton in a broad range of neuronal cell types and animal species. In: Proceedings of the National Academy of Sciences of the United States of America. 2016 ; Vol. 113, No. 21. pp. 6029-6034.
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AU - Kurshan, Peri T.

AU - Farley, Jonathan E.

AU - Simon, David J.

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AU - Han, Boran

AU - Hao, Junjie

AU - Heller, Evan

AU - Freeman, Marc R.

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