TY - JOUR
T1 - Prevalent presence of periodic actin-spectrin-based membrane skeleton in a broad range of neuronal cell types and animal species
AU - He, Jiang
AU - Zhou, Ruobo
AU - Wu, Zhuhao
AU - Carrasco, Monica A.
AU - Kurshan, Peri T.
AU - Farley, Jonathan E.
AU - Simon, David J.
AU - Wang, Guiping
AU - Han, Boran
AU - Hao, Junjie
AU - Heller, Evan
AU - Freeman, Marc R.
AU - Shen, Kang
AU - Maniatis, Tom
AU - Tessier-Lavigne, Marc
AU - Zhuang, Xiaowei
N1 - Funding Information:
The preprint of this paper has been posted on bioRxiv (dx.doi.org/10.1101/045856) for discussion and we thank a wide community of colleagues for participating in the discussion. This work is supported in part by the Howard Hughes Medical Institute (X.Z., K.S., and M.R.F.); National Institutes of Health Grants NS089786 (to M.T.-L.), NS048392 (to K.S.), and NS053538 (to M.R.F.); and the ALS Association (T.M.). R.Z. is an HHMI Fellow of the Life Sciences Research Foundation. Z.W. is supported in part by a Bristol-Myers Squibb Postdoctoral Fellowship at the Rockefeller University. X.Z., K.S., and M.R.F. are Howard Hughes Medical Institute investigators
PY - 2016/5/24
Y1 - 2016/5/24
N2 - 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.
AB - 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.
KW - Actin
KW - Cytoskeleton
KW - Neuron
KW - STORM
KW - Spectrin
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UR - http://www.scopus.com/inward/citedby.url?scp=84971421752&partnerID=8YFLogxK
U2 - 10.1073/pnas.1605707113
DO - 10.1073/pnas.1605707113
M3 - Article
C2 - 27162329
AN - SCOPUS:84971421752
SN - 0027-8424
VL - 113
SP - 6029
EP - 6034
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 21
ER -