Self-assembly of CIP4 drives actin-mediated asymmetric pit-closing in clathrin-mediated endocytosis
Abstract Clathrin-mediated endocytosis is pivotal to signal transduction pathways between the extracellular environment and the intracellular space. Evidence from live-cell imaging and super-resolution microscopy of mammalian cells suggests an asymmetric distribution of actin fibres near the clathri...
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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/s41467-023-40390-y |
| _version_ | 1797752672303972352 |
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| author | Yiming Yu Shige H. Yoshimura |
| author_facet | Yiming Yu Shige H. Yoshimura |
| author_sort | Yiming Yu |
| collection | DOAJ |
| description | Abstract Clathrin-mediated endocytosis is pivotal to signal transduction pathways between the extracellular environment and the intracellular space. Evidence from live-cell imaging and super-resolution microscopy of mammalian cells suggests an asymmetric distribution of actin fibres near the clathrin-coated pit, which induces asymmetric pit-closing rather than radial constriction. However, detailed molecular mechanisms of this ‘asymmetricity’ remain elusive. Herein, we used high-speed atomic force microscopy to demonstrate that CIP4, a multi-domain protein with a classic F-BAR domain and intrinsically disordered regions, is necessary for asymmetric pit-closing. Strong self-assembly of CIP4 via intrinsically disordered regions, together with stereospecific interactions with the curved membrane and actin-regulating proteins, generates a small actin-rich environment near the pit, which deforms the membrane and closes the pit. Our results provide mechanistic insights into how disordered and structured domain collaboration promotes spatio-temporal actin polymerisation near the plasma membrane. |
| first_indexed | 2024-03-12T17:06:47Z |
| format | Article |
| id | doaj.art-1378fef5066949688bbc60d134696408 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-12T17:06:47Z |
| publishDate | 2023-08-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-1378fef5066949688bbc60d1346964082023-08-06T11:19:12ZengNature PortfolioNature Communications2041-17232023-08-0114111510.1038/s41467-023-40390-ySelf-assembly of CIP4 drives actin-mediated asymmetric pit-closing in clathrin-mediated endocytosisYiming Yu0Shige H. Yoshimura1Graduate School of Biostudies, Kyoto UniversityGraduate School of Biostudies, Kyoto UniversityAbstract Clathrin-mediated endocytosis is pivotal to signal transduction pathways between the extracellular environment and the intracellular space. Evidence from live-cell imaging and super-resolution microscopy of mammalian cells suggests an asymmetric distribution of actin fibres near the clathrin-coated pit, which induces asymmetric pit-closing rather than radial constriction. However, detailed molecular mechanisms of this ‘asymmetricity’ remain elusive. Herein, we used high-speed atomic force microscopy to demonstrate that CIP4, a multi-domain protein with a classic F-BAR domain and intrinsically disordered regions, is necessary for asymmetric pit-closing. Strong self-assembly of CIP4 via intrinsically disordered regions, together with stereospecific interactions with the curved membrane and actin-regulating proteins, generates a small actin-rich environment near the pit, which deforms the membrane and closes the pit. Our results provide mechanistic insights into how disordered and structured domain collaboration promotes spatio-temporal actin polymerisation near the plasma membrane.https://doi.org/10.1038/s41467-023-40390-y |
| spellingShingle | Yiming Yu Shige H. Yoshimura Self-assembly of CIP4 drives actin-mediated asymmetric pit-closing in clathrin-mediated endocytosis Nature Communications |
| title | Self-assembly of CIP4 drives actin-mediated asymmetric pit-closing in clathrin-mediated endocytosis |
| title_full | Self-assembly of CIP4 drives actin-mediated asymmetric pit-closing in clathrin-mediated endocytosis |
| title_fullStr | Self-assembly of CIP4 drives actin-mediated asymmetric pit-closing in clathrin-mediated endocytosis |
| title_full_unstemmed | Self-assembly of CIP4 drives actin-mediated asymmetric pit-closing in clathrin-mediated endocytosis |
| title_short | Self-assembly of CIP4 drives actin-mediated asymmetric pit-closing in clathrin-mediated endocytosis |
| title_sort | self assembly of cip4 drives actin mediated asymmetric pit closing in clathrin mediated endocytosis |
| url | https://doi.org/10.1038/s41467-023-40390-y |
| work_keys_str_mv | AT yimingyu selfassemblyofcip4drivesactinmediatedasymmetricpitclosinginclathrinmediatedendocytosis AT shigehyoshimura selfassemblyofcip4drivesactinmediatedasymmetricpitclosinginclathrinmediatedendocytosis |