An Arp2/3 Nucleated F-Actin Shell Fragments Nuclear Membranes at Nuclear Envelope Breakdown in Starfish Oocytes
Animal cells disassemble and reassemble their nuclear envelopes (NEs) upon each division. Nuclear envelope breakdown (NEBD) serves as a major regulatory mechanism by which mixing of cytoplasmic and nuclear compartments drives the complete reorganization of cellular architecture, committing the cell...
| Main Authors: | , , , , , , , , |
|---|---|
| Other Authors: | |
| Format: | Article |
| Language: | en_US |
| Published: |
Elsevier
2014
|
| Online Access: | http://hdl.handle.net/1721.1/92376 https://orcid.org/0000-0002-6199-6855 |
| _version_ | 1811070034640896000 |
|---|---|
| author | Mori, Masashi Kondo, Hiroshi Monnier, Nilah Falk, Henning J. Machado, Pedro Bathe, Mark Somogyi, Kalman Nedelec, Francois Lenart, Peter |
| author2 | Massachusetts Institute of Technology. Department of Biological Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Biological Engineering Mori, Masashi Kondo, Hiroshi Monnier, Nilah Falk, Henning J. Machado, Pedro Bathe, Mark Somogyi, Kalman Nedelec, Francois Lenart, Peter |
| author_sort | Mori, Masashi |
| collection | MIT |
| description | Animal cells disassemble and reassemble their nuclear envelopes (NEs) upon each division. Nuclear envelope breakdown (NEBD) serves as a major regulatory mechanism by which mixing of cytoplasmic and nuclear compartments drives the complete reorganization of cellular architecture, committing the cell for division. Breakdown is initiated by phosphorylation-driven partial disassembly of the nuclear pore complexes (NPCs), increasing their permeability but leaving the overall NE structure intact. Subsequently, the NE is rapidly broken into membrane fragments, defining the transition from prophase to prometaphase and resulting in complete mixing of cyto- and nucleoplasm. However, the mechanism underlying this rapid NE fragmentation remains largely unknown. Here, we show that NE fragmentation during NEBD in starfish oocytes is driven by an Arp2/3 complex-nucleated F-actin “shell” that transiently polymerizes on the inner surface of the NE. Blocking the formation of this F-actin shell prevents membrane fragmentation and delays entry of large cytoplasmic molecules into the nucleus. We observe spike-like protrusions extending from the F-actin shell that appear to “pierce” the NE during the fragmentation process. Finally, we show that NE fragmentation is essential for successful reproduction, because blocking this process in meiosis leads to formation of aneuploid eggs. |
| first_indexed | 2024-09-23T08:21:29Z |
| format | Article |
| id | mit-1721.1/92376 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T08:21:29Z |
| publishDate | 2014 |
| publisher | Elsevier |
| record_format | dspace |
| spelling | mit-1721.1/923762022-09-30T09:08:59Z An Arp2/3 Nucleated F-Actin Shell Fragments Nuclear Membranes at Nuclear Envelope Breakdown in Starfish Oocytes Mori, Masashi Kondo, Hiroshi Monnier, Nilah Falk, Henning J. Machado, Pedro Bathe, Mark Somogyi, Kalman Nedelec, Francois Lenart, Peter Massachusetts Institute of Technology. Department of Biological Engineering Massachusetts Institute of Technology. Laboratory for Computational Cell Biology & Biophysics Bathe, Mark Monnier, Nilah Bathe, Mark Animal cells disassemble and reassemble their nuclear envelopes (NEs) upon each division. Nuclear envelope breakdown (NEBD) serves as a major regulatory mechanism by which mixing of cytoplasmic and nuclear compartments drives the complete reorganization of cellular architecture, committing the cell for division. Breakdown is initiated by phosphorylation-driven partial disassembly of the nuclear pore complexes (NPCs), increasing their permeability but leaving the overall NE structure intact. Subsequently, the NE is rapidly broken into membrane fragments, defining the transition from prophase to prometaphase and resulting in complete mixing of cyto- and nucleoplasm. However, the mechanism underlying this rapid NE fragmentation remains largely unknown. Here, we show that NE fragmentation during NEBD in starfish oocytes is driven by an Arp2/3 complex-nucleated F-actin “shell” that transiently polymerizes on the inner surface of the NE. Blocking the formation of this F-actin shell prevents membrane fragmentation and delays entry of large cytoplasmic molecules into the nucleus. We observe spike-like protrusions extending from the F-actin shell that appear to “pierce” the NE during the fragmentation process. Finally, we show that NE fragmentation is essential for successful reproduction, because blocking this process in meiosis leads to formation of aneuploid eggs. MIT Faculty Start-up Fund National Science Foundation (U.S.). Graduate Research Fellowship 2014-12-18T17:26:01Z 2014-12-18T17:26:01Z 2014-06 2014-05 Article http://purl.org/eprint/type/JournalArticle 09609822 1879-0445 http://hdl.handle.net/1721.1/92376 Mori, Masashi, Kalman Somogyi, Hiroshi Kondo, Nilah Monnier, Henning J. Falk, Pedro Machado, Mark Bathe, François Nedelec, and Peter Lenart. “An Arp2/3 Nucleated F-Actin Shell Fragments Nuclear Membranes at Nuclear Envelope Breakdown in Starfish Oocytes.” Current Biology 24, no. 12 (June 2014): 1421–1428. https://orcid.org/0000-0002-6199-6855 en_US http://dx.doi.org/10.1016/j.cub.2014.05.019 Current Biology Creative Commons Attribution-Noncommercial-Share Alike http://creativecommons.org/licenses/by-nc-sa/4.0/ application/pdf Elsevier Prof. Bathe via Howard Silver |
| spellingShingle | Mori, Masashi Kondo, Hiroshi Monnier, Nilah Falk, Henning J. Machado, Pedro Bathe, Mark Somogyi, Kalman Nedelec, Francois Lenart, Peter An Arp2/3 Nucleated F-Actin Shell Fragments Nuclear Membranes at Nuclear Envelope Breakdown in Starfish Oocytes |
| title | An Arp2/3 Nucleated F-Actin Shell Fragments Nuclear Membranes at Nuclear Envelope Breakdown in Starfish Oocytes |
| title_full | An Arp2/3 Nucleated F-Actin Shell Fragments Nuclear Membranes at Nuclear Envelope Breakdown in Starfish Oocytes |
| title_fullStr | An Arp2/3 Nucleated F-Actin Shell Fragments Nuclear Membranes at Nuclear Envelope Breakdown in Starfish Oocytes |
| title_full_unstemmed | An Arp2/3 Nucleated F-Actin Shell Fragments Nuclear Membranes at Nuclear Envelope Breakdown in Starfish Oocytes |
| title_short | An Arp2/3 Nucleated F-Actin Shell Fragments Nuclear Membranes at Nuclear Envelope Breakdown in Starfish Oocytes |
| title_sort | arp2 3 nucleated f actin shell fragments nuclear membranes at nuclear envelope breakdown in starfish oocytes |
| url | http://hdl.handle.net/1721.1/92376 https://orcid.org/0000-0002-6199-6855 |
| work_keys_str_mv | AT morimasashi anarp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT kondohiroshi anarp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT monniernilah anarp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT falkhenningj anarp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT machadopedro anarp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT bathemark anarp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT somogyikalman anarp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT nedelecfrancois anarp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT lenartpeter anarp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT morimasashi arp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT kondohiroshi arp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT monniernilah arp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT falkhenningj arp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT machadopedro arp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT bathemark arp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT somogyikalman arp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT nedelecfrancois arp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes AT lenartpeter arp23nucleatedfactinshellfragmentsnuclearmembranesatnuclearenvelopebreakdowninstarfishoocytes |