Switch of cell migration modes orchestrated by changes of three-dimensional lamellipodium structure and intracellular diffusion
Abstract Cell migration plays important roles in many biological processes, but how migrating cells orchestrate intracellular molecules and subcellular structures to regulate their speed and direction is still not clear. Here, by characterizing the intracellular diffusion and the three-dimensional l...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-08-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-40858-x |
| _version_ | 1827709579454054400 |
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| author | Chao Jiang Hong-Yu Luo Xinpeng Xu Shuo-Xing Dou Wei Li Dongshi Guan Fangfu Ye Xiaosong Chen Ming Guo Peng-Ye Wang Hui Li |
| author_facet | Chao Jiang Hong-Yu Luo Xinpeng Xu Shuo-Xing Dou Wei Li Dongshi Guan Fangfu Ye Xiaosong Chen Ming Guo Peng-Ye Wang Hui Li |
| author_sort | Chao Jiang |
| collection | DOAJ |
| description | Abstract Cell migration plays important roles in many biological processes, but how migrating cells orchestrate intracellular molecules and subcellular structures to regulate their speed and direction is still not clear. Here, by characterizing the intracellular diffusion and the three-dimensional lamellipodium structures of fish keratocyte cells, we observe a strong positive correlation between the intracellular diffusion and cell migration speed and, more importantly, discover a switching of cell migration modes with reversible intracellular diffusion variation and lamellipodium structure deformation. Distinct from the normal fast mode, cells migrating in the newly-found slow mode have a deformed lamellipodium with swollen-up front and thinned-down rear, reduced intracellular diffusion and compartmentalized macromolecule distribution in the lamellipodium. Furthermore, in turning cells, both lamellipodium structure and intracellular diffusion dynamics are also changed, with left-right symmetry breaking. We propose a mechanism involving the front-localized actin polymerization and increased molecular crowding in the lamellipodium to explain how cells spatiotemporally coordinate the intracellular diffusion dynamics and the lamellipodium structure in regulating their migrations. |
| first_indexed | 2024-03-10T17:23:57Z |
| format | Article |
| id | doaj.art-f75cd0760c1a47b0a47803134da555d7 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-10T17:23:57Z |
| publishDate | 2023-08-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-f75cd0760c1a47b0a47803134da555d72023-11-20T10:16:14ZengNature PortfolioNature Communications2041-17232023-08-0114111310.1038/s41467-023-40858-xSwitch of cell migration modes orchestrated by changes of three-dimensional lamellipodium structure and intracellular diffusionChao Jiang0Hong-Yu Luo1Xinpeng Xu2Shuo-Xing Dou3Wei Li4Dongshi Guan5Fangfu Ye6Xiaosong Chen7Ming Guo8Peng-Ye Wang9Hui Li10Beijing National Laboratory for Condensed Matter Physics and Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of SciencesBeijing National Laboratory for Condensed Matter Physics and Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of SciencesPhysics Program, Guangdong Technion—Israel Institute of TechnologyBeijing National Laboratory for Condensed Matter Physics and Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of SciencesBeijing National Laboratory for Condensed Matter Physics and Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of SciencesSchool of Physical Sciences and School of Engineering Sciences, University of Chinese Academy of SciencesBeijing National Laboratory for Condensed Matter Physics and Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of SciencesSchool of Systems Science and Institute of Nonequilibrium Systems, Beijing Normal UniversityDepartment of Mechanical Engineering, MIT, 77 Massachusetts AveBeijing National Laboratory for Condensed Matter Physics and Laboratory of Soft Matter Physics, Institute of Physics, Chinese Academy of SciencesSchool of Systems Science and Institute of Nonequilibrium Systems, Beijing Normal UniversityAbstract Cell migration plays important roles in many biological processes, but how migrating cells orchestrate intracellular molecules and subcellular structures to regulate their speed and direction is still not clear. Here, by characterizing the intracellular diffusion and the three-dimensional lamellipodium structures of fish keratocyte cells, we observe a strong positive correlation between the intracellular diffusion and cell migration speed and, more importantly, discover a switching of cell migration modes with reversible intracellular diffusion variation and lamellipodium structure deformation. Distinct from the normal fast mode, cells migrating in the newly-found slow mode have a deformed lamellipodium with swollen-up front and thinned-down rear, reduced intracellular diffusion and compartmentalized macromolecule distribution in the lamellipodium. Furthermore, in turning cells, both lamellipodium structure and intracellular diffusion dynamics are also changed, with left-right symmetry breaking. We propose a mechanism involving the front-localized actin polymerization and increased molecular crowding in the lamellipodium to explain how cells spatiotemporally coordinate the intracellular diffusion dynamics and the lamellipodium structure in regulating their migrations.https://doi.org/10.1038/s41467-023-40858-x |
| spellingShingle | Chao Jiang Hong-Yu Luo Xinpeng Xu Shuo-Xing Dou Wei Li Dongshi Guan Fangfu Ye Xiaosong Chen Ming Guo Peng-Ye Wang Hui Li Switch of cell migration modes orchestrated by changes of three-dimensional lamellipodium structure and intracellular diffusion Nature Communications |
| title | Switch of cell migration modes orchestrated by changes of three-dimensional lamellipodium structure and intracellular diffusion |
| title_full | Switch of cell migration modes orchestrated by changes of three-dimensional lamellipodium structure and intracellular diffusion |
| title_fullStr | Switch of cell migration modes orchestrated by changes of three-dimensional lamellipodium structure and intracellular diffusion |
| title_full_unstemmed | Switch of cell migration modes orchestrated by changes of three-dimensional lamellipodium structure and intracellular diffusion |
| title_short | Switch of cell migration modes orchestrated by changes of three-dimensional lamellipodium structure and intracellular diffusion |
| title_sort | switch of cell migration modes orchestrated by changes of three dimensional lamellipodium structure and intracellular diffusion |
| url | https://doi.org/10.1038/s41467-023-40858-x |
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