Developmental mechanism of the periodic membrane skeleton in axons
Actin, spectrin, and associated molecules form a periodic sub-membrane lattice structure in axons. How this membrane skeleton is developed and why it preferentially forms in axons are unknown. Here, we studied the developmental mechanism of this lattice structure. We found that this structure emerge...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2014-12-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/04581 |
| _version_ | 1811200375991042048 |
|---|---|
| author | Guisheng Zhong Jiang He Ruobo Zhou Damaris Lorenzo Hazen P Babcock Vann Bennett Xiaowei Zhuang |
| author_facet | Guisheng Zhong Jiang He Ruobo Zhou Damaris Lorenzo Hazen P Babcock Vann Bennett Xiaowei Zhuang |
| author_sort | Guisheng Zhong |
| collection | DOAJ |
| description | Actin, spectrin, and associated molecules form a periodic sub-membrane lattice structure in axons. How this membrane skeleton is developed and why it preferentially forms in axons are unknown. Here, we studied the developmental mechanism of this lattice structure. We found that this structure emerged early during axon development and propagated from proximal regions to distal ends of axons. Components of the axon initial segment were recruited to the lattice late during development. Formation of the lattice was regulated by the local concentration of βII spectrin, which is higher in axons than in dendrites. Increasing the dendritic concentration of βII spectrin by overexpression or by knocking out ankyrin B induced the formation of the periodic structure in dendrites, demonstrating that the spectrin concentration is a key determinant in the preferential development of this structure in axons and that ankyrin B is critical for the polarized distribution of βII spectrin in neurites. |
| first_indexed | 2024-04-12T02:03:52Z |
| format | Article |
| id | doaj.art-93e491f51f9a4d62b83197bc780ce54f |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:03:52Z |
| publishDate | 2014-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-93e491f51f9a4d62b83197bc780ce54f2022-12-22T03:52:37ZengeLife Sciences Publications LtdeLife2050-084X2014-12-01310.7554/eLife.04581Developmental mechanism of the periodic membrane skeleton in axonsGuisheng Zhong0Jiang He1Ruobo Zhou2Damaris Lorenzo3Hazen P Babcock4Vann Bennett5Xiaowei Zhuang6Department of Chemistry and Chemical Biology, Howard Hughes Medical Institute, Harvard University, Cambridge, United StatesDepartment of Molecular and Cellular Biology, Howard Hughes Medical Institute, Harvard University, Cambridge, United StatesDepartment of Chemistry and Chemical Biology, Howard Hughes Medical Institute, Harvard University, Cambridge, United StatesDepartment of Biochemistry, Duke University, Durham, United States; Department of Neurobiology, Duke University, Durham, United StatesCenter for Brain Sciences, Harvard University, Cambridge, United StatesDepartment of Neurobiology, Duke University, Durham, United States; Department of Biochemistry, Howard Hughes Medical Institute, Duke University, Durham, United StatesDepartment of Chemistry and Chemical Biology, Howard Hughes Medical Institute, Harvard University, Cambridge, United States; Department of Physics, Harvard University, Cambridge, United StatesActin, spectrin, and associated molecules form a periodic sub-membrane lattice structure in axons. How this membrane skeleton is developed and why it preferentially forms in axons are unknown. Here, we studied the developmental mechanism of this lattice structure. We found that this structure emerged early during axon development and propagated from proximal regions to distal ends of axons. Components of the axon initial segment were recruited to the lattice late during development. Formation of the lattice was regulated by the local concentration of βII spectrin, which is higher in axons than in dendrites. Increasing the dendritic concentration of βII spectrin by overexpression or by knocking out ankyrin B induced the formation of the periodic structure in dendrites, demonstrating that the spectrin concentration is a key determinant in the preferential development of this structure in axons and that ankyrin B is critical for the polarized distribution of βII spectrin in neurites.https://elifesciences.org/articles/04581actinspectrinankyrinaxonsuper-resolutionSTORM |
| spellingShingle | Guisheng Zhong Jiang He Ruobo Zhou Damaris Lorenzo Hazen P Babcock Vann Bennett Xiaowei Zhuang Developmental mechanism of the periodic membrane skeleton in axons eLife actin spectrin ankyrin axon super-resolution STORM |
| title | Developmental mechanism of the periodic membrane skeleton in axons |
| title_full | Developmental mechanism of the periodic membrane skeleton in axons |
| title_fullStr | Developmental mechanism of the periodic membrane skeleton in axons |
| title_full_unstemmed | Developmental mechanism of the periodic membrane skeleton in axons |
| title_short | Developmental mechanism of the periodic membrane skeleton in axons |
| title_sort | developmental mechanism of the periodic membrane skeleton in axons |
| topic | actin spectrin ankyrin axon super-resolution STORM |
| url | https://elifesciences.org/articles/04581 |
| work_keys_str_mv | AT guishengzhong developmentalmechanismoftheperiodicmembraneskeletoninaxons AT jianghe developmentalmechanismoftheperiodicmembraneskeletoninaxons AT ruobozhou developmentalmechanismoftheperiodicmembraneskeletoninaxons AT damarislorenzo developmentalmechanismoftheperiodicmembraneskeletoninaxons AT hazenpbabcock developmentalmechanismoftheperiodicmembraneskeletoninaxons AT vannbennett developmentalmechanismoftheperiodicmembraneskeletoninaxons AT xiaoweizhuang developmentalmechanismoftheperiodicmembraneskeletoninaxons |