Growth cone-localized microtubule organizing center establishes microtubule orientation in dendrites
A polarized arrangement of neuronal microtubule arrays is the foundation of membrane trafficking and subcellular compartmentalization. Conserved among both invertebrates and vertebrates, axons contain exclusively ‘plus-end-out’ microtubules while dendrites contain a high percentage of ‘minus-end-out...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2020-07-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/56547 |
| _version_ | 1811181081506873344 |
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| author | Xing Liang Marcela Kokes Richard D Fetter Maria Danielle Sallee Adrian W Moore Jessica L Feldman Kang Shen |
| author_facet | Xing Liang Marcela Kokes Richard D Fetter Maria Danielle Sallee Adrian W Moore Jessica L Feldman Kang Shen |
| author_sort | Xing Liang |
| collection | DOAJ |
| description | A polarized arrangement of neuronal microtubule arrays is the foundation of membrane trafficking and subcellular compartmentalization. Conserved among both invertebrates and vertebrates, axons contain exclusively ‘plus-end-out’ microtubules while dendrites contain a high percentage of ‘minus-end-out’ microtubules, the origins of which have been a mystery. Here we show that in Caenorhabditis elegans the dendritic growth cone contains a non-centrosomal microtubule organizing center (MTOC), which generates minus-end-out microtubules along outgrowing dendrites and plus-end-out microtubules in the growth cone. RAB-11-positive endosomes accumulate in this region and co-migrate with the microtubule nucleation complex γ-TuRC. The MTOC tracks the extending growth cone by kinesin-1/UNC-116-mediated endosome movements on distal plus-end-out microtubules and dynein clusters this advancing MTOC. Critically, perturbation of the function or localization of the MTOC causes reversed microtubule polarity in dendrites. These findings unveil the endosome-localized dendritic MTOC as a critical organelle for establishing axon-dendrite polarity. |
| first_indexed | 2024-04-11T09:13:49Z |
| format | Article |
| id | doaj.art-53ff6b0e9f694e06bf5a746857c9ab01 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:13:49Z |
| publishDate | 2020-07-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-53ff6b0e9f694e06bf5a746857c9ab012022-12-22T04:32:25ZengeLife Sciences Publications LtdeLife2050-084X2020-07-01910.7554/eLife.56547Growth cone-localized microtubule organizing center establishes microtubule orientation in dendritesXing Liang0https://orcid.org/0000-0002-8298-1214Marcela Kokes1https://orcid.org/0000-0002-7218-481XRichard D Fetter2https://orcid.org/0000-0002-1558-100XMaria Danielle Sallee3Adrian W Moore4Jessica L Feldman5https://orcid.org/0000-0002-5210-5045Kang Shen6https://orcid.org/0000-0003-4059-8249Department of Biology, Stanford University, Stanford, United States; Howard Hughes Medical Institute, Stanford University, Stanford, United StatesDepartment of Biology, Stanford University, Stanford, United States; Howard Hughes Medical Institute, Stanford University, Stanford, United StatesHoward Hughes Medical Institute, Stanford University, Stanford, United StatesDepartment of Biology, Stanford University, Stanford, United StatesRIKEN Center for Brain Science, Wako, JapanDepartment of Biology, Stanford University, Stanford, United StatesDepartment of Biology, Stanford University, Stanford, United States; Howard Hughes Medical Institute, Stanford University, Stanford, United StatesA polarized arrangement of neuronal microtubule arrays is the foundation of membrane trafficking and subcellular compartmentalization. Conserved among both invertebrates and vertebrates, axons contain exclusively ‘plus-end-out’ microtubules while dendrites contain a high percentage of ‘minus-end-out’ microtubules, the origins of which have been a mystery. Here we show that in Caenorhabditis elegans the dendritic growth cone contains a non-centrosomal microtubule organizing center (MTOC), which generates minus-end-out microtubules along outgrowing dendrites and plus-end-out microtubules in the growth cone. RAB-11-positive endosomes accumulate in this region and co-migrate with the microtubule nucleation complex γ-TuRC. The MTOC tracks the extending growth cone by kinesin-1/UNC-116-mediated endosome movements on distal plus-end-out microtubules and dynein clusters this advancing MTOC. Critically, perturbation of the function or localization of the MTOC causes reversed microtubule polarity in dendrites. These findings unveil the endosome-localized dendritic MTOC as a critical organelle for establishing axon-dendrite polarity.https://elifesciences.org/articles/56547neuronal cell polaritydendrite developmentmicrotubule organizationacentrosomal mtocγ-TuRC |
| spellingShingle | Xing Liang Marcela Kokes Richard D Fetter Maria Danielle Sallee Adrian W Moore Jessica L Feldman Kang Shen Growth cone-localized microtubule organizing center establishes microtubule orientation in dendrites eLife neuronal cell polarity dendrite development microtubule organization acentrosomal mtoc γ-TuRC |
| title | Growth cone-localized microtubule organizing center establishes microtubule orientation in dendrites |
| title_full | Growth cone-localized microtubule organizing center establishes microtubule orientation in dendrites |
| title_fullStr | Growth cone-localized microtubule organizing center establishes microtubule orientation in dendrites |
| title_full_unstemmed | Growth cone-localized microtubule organizing center establishes microtubule orientation in dendrites |
| title_short | Growth cone-localized microtubule organizing center establishes microtubule orientation in dendrites |
| title_sort | growth cone localized microtubule organizing center establishes microtubule orientation in dendrites |
| topic | neuronal cell polarity dendrite development microtubule organization acentrosomal mtoc γ-TuRC |
| url | https://elifesciences.org/articles/56547 |
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