Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing

Nature

Volumn 522, Issue 7555, 2015, Pages 231-235

  Vietri, Marina ^a,b   Schink, Kay O ^a,b   Campsteijn, Coen ^a,b   Wegner, Catherine Sem ^a,b   Schultz, Sebastian W ^a,b   Christ, Liliane ^a,b   Thoresen, Sigrid B ^a,b   Brech, Andreas ^a,b   Raiborg, Camilla ^a,b   Stenmark, Harald ^a,b,c  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE VPS4; ESCRT III PROTEIN; ESCRT PROTEIN; SPASTIN; UNCLASSIFIED DRUG; CHROMATIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SPAST PROTEIN, HUMAN; VPS4A PROTEIN, HUMAN;

ABSCISSION; CELL ORGANELLE; CHROMOSOME; ENZYME ACTIVITY; GENOME; MEMBRANE; METAZOAN; PROTEIN; VIRUS;

ANAPHASE; ARTICLE; CELL MEMBRANE; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; CYTOKINESIS; DNA DAMAGE; FEMALE; GENOME; HUMAN; HUMAN CELL; MICROTUBULE; MITOSIS SPINDLE; PRIORITY JOURNAL; VIRUS RELEASE; CELL CYCLE CHECKPOINT; CHROMATIN; GENETICS; MEMBRANE FUSION; METABOLISM; SPINDLE APPARATUS;

METAZOA;

ADENOSINE TRIPHOSPHATASES; ANAPHASE; CELL CYCLE CHECKPOINTS; CHROMATIN; DNA DAMAGE; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HUMANS; MEMBRANE FUSION; MICROTUBULES; NUCLEAR ENVELOPE; SPINDLE APPARATUS; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84930946081     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14408     Document Type: Article

References (41)

1. Guttinger, S., Laurell, E. , Kutay, U. Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nature Rev. Mol. Cell Biol. 10, 178-191 (2009).
2. Burke, B. , Ellenberg, J. Remodelling the walls of the nucleus. Nature Rev. Mol. Cell Biol. 3, 487-497 (2002).
3. Babst, M., Katzmann, D. J., Estepa-Sabal, E. J., Meerloo, T. , Emr, S. D. Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev. Cell 3, 271-282 (2002).
4. von Schwedler, U. K. et al. The protein network of HIV budding. Cell 114, 701-713 (2003).
5. Carlton, J. G. , Martin-Serrano, J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908-1912 (2007).
6. Jimenez, A. J. et al. ESCRT machinery is required for plasma membrane repair. Science 343, 1247136 (2014).
7. Guizetti, J. et al. Cortical constriction during abscission involves helices of ESCRTIII-dependent filaments. Science 331, 1616-1620 (2011).
8. Morita, E. et al. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 26, 4215-4227 (2007).
9. Poser, I. et al. BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. Nature Methods 5, 409-415 (2008).
10. Hanson, P. I., Roth, R., Lin, Y. , Heuser, J. E. Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J. Cell Biol. 180, 389-402 (2008).
11. Hetzer, M. W. The nuclear envelope. Cold Spring Harb. Perspect. Biol. 2, a000539 (2010).
12. Wollert, T., Wunder, C., Lippincott-Schwartz, J. , Hurley, J. H. Membrane scission by the ESCRT-III complex. Nature 458, 172-177 (2009).
13. Stauffer, D. R., Howard, T. L., Nyun, T.& Hollenberg, S. M.CHMP1 is a novel nuclear matrix protein affecting chromatin structure and cell-cycle progression. J. Cell Sci. 114, 2383-2393 (2001).
14. Buchkovich, N. J., Henne, W. M., Tang, S.and Emr, S. D. Essential N-terminal insertion motif anchors the ESCRT-III filament during MVB vesicle formation. Dev. Cell 27, 201-214 (2013).
15. Henne, W. M., Stenmark, H. , Emr, S. D. Molecular mechanisms of the membrane sculpting ESCRT pathway. Cold Spring Harb. Perspect. Biol. 5, http://dx.doi.org/10.1101/cshperspect.a016766 (2013).
16. Horii, M. et al. CHMP7, a novel ESCRT-III-related protein, associates with CHMP4b and functions in the endosomal sorting pathway. Biochem. J. 400, 23-32 (2006).
17. Hill, C. P. , Babst, M. Structure and function of the membrane deformation AAA ATPase Vps4. Biochim. Biophys. Acta 1823, 172-181 (2012).
18. Haraguchi, T. et al. Live cell imaging and electron microscopy reveal dynamic processes ofBAF-directednuclear envelope assembly. J.Cell Sci.121, 2540-2554 (2008).
19. Lu, L., Ladinsky, M. S. , Kirchhausen, T. Formation of the postmitotic nuclear envelope fromextended ER cisternae precedes nuclear pore assembly. J. Cell Biol. 194, 425-440 (2011).
20. Yang, D. et al. Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nature Struct. Mol. Biol. 15, 1278-1286 (2008).
21. Lumb, J. H., Connell, J. W., Allison, R. , Reid, E. The AAA ATPase spastin links microtubule severing to membrane modelling. Biochim. Biophys. Acta 1823, 192-197 (2012).
22. Agromayor, M. et al. Essential role of hIST1 in cytokinesis. Mol. Biol. Cell 20, 1374-1387 (2009).
23. Reid, E. et al. The hereditary spastic paraplegia protein spastin interacts with the ESCRT-III complex-associated endosomal protein CHMP1B. Hum. Mol. Genet. 14, 19-38 (2005).
24. Lattanzi, G., Marmiroli, S., Facchini, A. , Maraldi, N. M. Nuclear damages and oxidative stress: new perspectives for laminopathies. Eur. J. Histochem. 56, e45 (2012).
25. Liu, B. et al. Genomic instability in laminopathy-based premature aging. Nature Med. 11, 780-785 (2005).
26. Abbas, T. , Dutta, A. p21 in cancer: intricate networks and multiple activities. Nature Rev. Cancer 9, 400-414 (2009).
27. Hatch, E. , Hetzer, M. Breaching the nuclear envelope in development and disease. J. Cell Biol. 205, 133-141 (2014).
28. Steigemann, P. et al. Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 136, 473-484 (2009).
29. Carlton, J. G., Caballe, A., Agromayor, M., Kloc, M. , Martin-Serrano, J. ESCRT-III governs the Aurora B-mediated abscission checkpoint through CHMP4C. Science 336, 220-225 (2012).
30. Thoresen, S. B. et al. ANCHR mediates Aurora-B-dependent abscission checkpoint control through retention of VPS4. Nature Cell Biol. 16, 550-560 (2014).
31. Bache, K. G. et al.The ESCRT-III subunit hVps24is required for degradationbut not silencing of the epidermal growth factor receptor. Mol. Biol. Cell 17, 2513-2523 (2006).
32. Sagona, A. P. et al. PtdIns(3)P controls cytokinesis through KIF13A-mediated recruitment of FYVE-CENT to the midbody. Nature Cell Biol. 12, 362-371 (2010).
33. Mu, F. T. et al. EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine "fingers" and contains a calmodulin-binding IQmotif. J. Biol. Chem. 270, 13503-13511 (1995).
34. Raiborg, C., Bache, K. G., Mehlum, A., Stang, E. , Stenmark, H. Hrs recruits clathrin to early endosomes. EMBO J. 20, 5008-5021 (2001).
35. Schmitz, M. H. et al. Live-cell imaging RNAi screen identifies PP2A-B55alpha and importin-beta1 as key mitotic exit regulators in human cells. Nature Cell Biol. 12, 886-893 (2010).
36. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nature Methods 9, 676-682 (2012).
37. McKinney, W. Data structures for statistical computing in Python. In Proc. 9th Python in Science Conference 51-56 (2010).
38. Dultz, E., Huet, S. , Ellenberg, J. Formation of the nuclear envelope permeability barrier studied by sequential photoswitching and flux analysis. Biophys. J. 97, 1891-1897 (2009).
39. Campeau, E. et al. A versatile viral system for expression and depletion of proteins in mammalian cells. PLoS ONE 4, e6529 (2009).
40. Dull, T. et al. A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72, 8463-8471 (1998).
41. Kremer, J. R. et al. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76 (1996).