title: Prevalent presence of periodic actin-spectrin-based membrane skeleton in a broad range of neuronal cell types and animal species.
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.
authors.affiliation: Howard Hughes Medical Institute, Harvard University, Cambridge, MA 02138; Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA 02138; Department of Physics, Harvard University, Cambridge, MA 02138;
authors.forename: Jiang
authors.initials: J
authors.lastname: He
authors.affiliation: Howard Hughes Medical Institute, Harvard University, Cambridge, MA 02138; Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA 02138; Department of Physics, Harvard University, Cambridge, MA 02138;
authors.forename: Ruobo
authors.initials: R
authors.lastname: Zhou
authors.affiliation: Laboratory of Brain Development and Repair, The Rockefeller University, New York, NY 10065;
authors.forename: Zhuhao
authors.initials: Z
authors.lastname: Wu
authors.affiliation: Department of Biochemistry and Molecular Biophysics, Columbia University Medical Center, New York, NY 10032;
authors.forename: Monica A
authors.initials: MA
authors.lastname: Carrasco
authors.affiliation: Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305; Department of Biology, Stanford University, Stanford, CA 94305;
authors.forename: Peri T
authors.initials: PT
authors.lastname: Kurshan
authors.affiliation: Howard Hughes Medical Institute, University of Massachusetts Medical School, Worcester, MA 01605; Department of Neurobiology, University of Massachusetts Medical School, Worcester, MA 01605.
authors.forename: Jonathan E
authors.initials: JE
authors.lastname: Farley
authors.affiliation: Laboratory of Brain Development and Repair, The Rockefeller University, New York, NY 10065;
authors.forename: David J
authors.initials: DJ
authors.lastname: Simon
authors.affiliation: Howard Hughes Medical Institute, Harvard University, Cambridge, MA 02138; Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA 02138; Department of Physics, Harvard University, Cambridge, MA 02138;
authors.forename: Guiping
authors.initials: G
authors.lastname: Wang
authors.affiliation: Howard Hughes Medical Institute, Harvard University, Cambridge, MA 02138; Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA 02138; Department of Physics, Harvard University, Cambridge, MA 02138;
authors.forename: Boran
authors.initials: B
authors.lastname: Han
authors.affiliation: Howard Hughes Medical Institute, Harvard University, Cambridge, MA 02138; Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA 02138; Department of Physics, Harvard University, Cambridge, MA 02138;
authors.forename: Junjie
authors.initials: J
authors.lastname: Hao
authors.affiliation: Howard Hughes Medical Institute, Harvard University, Cambridge, MA 02138; Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA 02138; Department of Physics, Harvard University, Cambridge, MA 02138;
authors.forename: Evan
authors.initials: E
authors.lastname: Heller
authors.affiliation: Howard Hughes Medical Institute, University of Massachusetts Medical School, Worcester, MA 01605; Department of Neurobiology, University of Massachusetts Medical School, Worcester, MA 01605.
authors.forename: Marc R
authors.initials: MR
authors.lastname: Freeman
authors.affiliation: Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305; Department of Biology, Stanford University, Stanford, CA 94305;
authors.forename: Kang
authors.initials: K
authors.lastname: Shen
authors.affiliation: Department of Biochemistry and Molecular Biophysics, Columbia University Medical Center, New York, NY 10032;
authors.forename: Tom
authors.initials: T
authors.lastname: Maniatis
authors.affiliation: Laboratory of Brain Development and Repair, The Rockefeller University, New York, NY 10065;
authors.forename: Marc
authors.initials: M
authors.lastname: Tessier-Lavigne
authors.affiliation: Howard Hughes Medical Institute, Harvard University, Cambridge, MA 02138; Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA 02138; Department of Physics, Harvard University, Cambridge, MA 02138; zhuang@chemistry.harvard.edu.
authors.forename: Xiaowei
authors.identifier: 0000-0002-6034-7853
authors.initials: X
authors.lastname: Zhuang
mesh_terms: D000199:Actins / Q000235:genetics / Q000378:metabolism*; D000818:Animals; D001369:Axons / Q000378:metabolism*; D017173:Caenorhabditis elegans; D002460:Cell Line; D002462:Cell Membrane / Q000235:genetics / Q000378:metabolism*; D002645:Chickens; D003599:Cytoskeleton / Q000235:genetics / Q000378:metabolism*; D003712:Dendrites / Q000235:genetics / Q000378:metabolism*; D004331:Drosophila melanogaster; D051379:Mice; D013045:Species Specificity; D013049:Spectrin / Q000235:genetics / Q000378:metabolism*
chemical_list: D000199:Actins; D013049:Spectrin
keywords: STORM; actin; cytoskeleton; neuron; spectrin