Cdc48/p97 promotes reformation of the nucleus by extracting the kinase Aurora B from chromatin
Open accessAbstract
During division of metazoan cells, the nucleus disassembles to allow chromosome segregation, and then reforms in each daughter cell. Reformation of the nucleus involves chromatin decondensation and assembly of the double-membrane nuclear envelope around the chromatin; however, regulation of the process is still poorly understood. In vitro, nucleus formation requires p97 (ref. 3), a hexameric ATPase implicated in membrane fusion and ubiquitin-dependent processes. However, the role and relevance of p97 in nucleus formation have remained controversial. Here we show that p97 stimulates nucleus reformation by inactivating the chromatin-associated kinase Aurora B. During mitosis, Aurora B inhibits nucleus reformation by preventing chromosome decondensation and formation of the nuclear envelope membrane. During exit from mitosis, p97 binds to Aurora B after its ubiquitylation and extracts it from chromatin. This leads to inactivation of Aurora B on chromatin, thus allowing chromatin decondensation and nuclear envelope formation. These data reveal an essential pathway that regulates reformation of the nucleus after mitosis and defines ubiquitin-dependent protein extraction as a common mechanism of Cdc48/p97 activity also during nucleus formation.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
AAA+ ATPase p97 unfoldase activity is necessary for extracting a subset of proteins marked for degradation from multi-protein complexes, chromatin, or membrane bound complexes.
“AAA+ ATPase p97 unfoldase activity has been demonstrated to be necessary for extracting a subset of proteins marked for degradation from multi-protein complexes, chromatin, or membrane bound complexes (Ramadan et al., 2007; Shcherbik and Haines, 2007; Verma et al., 2011).”
From Mapping the Degradable Kinome Provides a Resource for Expedited Degrader Development (2020) · cites this paper as Ramadan et al., 2007
Cites
Systematic functional analysis of the Caenorhabditis elegans genome using RNAi
Kamath, R. S., Fraser, A. G., Yan, D., Poulin, G. B., Durbin, R. M., Gotta, M., Kanapin, A. A., Bot, N. L., Moreno, S., Sohrmann, M., et al. (2003) · Nature · doi:10.1038/nature01278 · Cited by 3,542 · see citing works
Self-citationERAD: the long road to destruction
Meusser, B., Hirsch, C., Jarosch, E., & Sommer, T. (2005) · Nature Cell Biology · doi:10.1038/ncb0805-766 · Cited by 1,221 · see citing works
Hauf, S., Cole, R. W., Terra, S. L., Zimmer, C., Schnapp, G., Walter, R., Heckel, A., Meel, J. C. A. V., Rieder, C. L., & Peters, J. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200208092 · Cited by 1,160 · see citing works
Regulation of HP1–chromatin binding by histone H3 methylation and phosphorylation
Fischle, W., Tseng, B. S., Dormann, H. L., Ueberheide, B. M., Garcia, B. A., Shabanowitz, J., Hunt, D. F., Funabiki, H., & Allis, C. D. (2005) · Nature · doi:10.1038/nature04219 · Cited by 996 · see citing works
Chapter 30 Cell Cycle Extracts
Murray, A. W. (1991) · Methods in cell biology · doi:10.1016/s0091-679x(08)60298-8 · Cited by 942 · see citing works
Hsu, J.-Y., Sun, Z., Li, X., Reuben, M., Tatchell, K., Bishop, D. K., Grushcow, J. M., Brame, C. J., Caldwell, J., Hunt, D. F., et al. (2000) · Cell · doi:10.1016/s0092-8674(00)00034-9 · Cited by 861 · see citing works
Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin
Hirota, T., Lipp, J., Toh, B., & Peters, J. (2005) · Nature · doi:10.1038/nature04254 · Cited by 662 · see citing works
Function of the p97–Ufd1–Npl4 complex in retrotranslocation from the ER to the cytosol
Ye, Y., Meyer, H. H., & Rapoport, T. A. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200302169 · Cited by 598 · see citing works
Self-citationMeyer, H. H., Shorter, J., Seemann, J., Pappin, D., & Warren, G. (2000) · The EMBO Journal · doi:10.1093/emboj/19.10.2181 · Cited by 446 · see citing works
Self-citationp47 is a cofactor for p97-mediated membrane fusion
Kondo, H., Rabouille, C., Newman, R., Levine, T. P., Pappin, D., Freemont, P. S., & Warren, G. (1997) · Nature · doi:10.1038/40411 · Cited by 437 · see citing works
Mechanism of Aurora B Activation by INCENP and Inhibition by Hesperadin
Sessa, F., Mapelli, M., Ciferri, C., Tarricone, C., Areces, L. B., Schneider, T. R., Stukenberg, P. T., & Musacchio, A. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.03.031 · Cited by 387 · see citing works
Hagstrom, K., Holmes, V., Cozzarelli, N., & Meyer, B. J. (2002) · Genes & Development · doi:10.1101/gad.968302 · Cited by 350 · see citing works
Chromosomal passengers: the four-dimensional regulation of mitotic events
Vagnarelli, P., & Earnshaw, W. C. (2004) · Chromosoma · doi:10.1007/s00412-004-0307-3 · Cited by 314 · see citing works
Distinct AAA-ATPase p97 complexes function in discrete steps of nuclear assembly
Hetzer, M. W., Meyer, H. H., Walther, T. C., Bilbao, D., Warren, G., & Mattaj, I. W. (2001) · Nature Cell Biology · doi:10.1038/ncb1201-1086 · Cited by 311 · see citing works
Self-citationPUSHING THE ENVELOPE: Structure, Function, and Dynamics of the Nuclear Periphery
Hetzer, M. W., Walther, T. C., & Mattaj, I. W. (2005) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.21.090704.151152 · Cited by 298 · see citing works
Cdc48 (p97): a ‘molecular gearbox’ in the ubiquitin pathway?
Jentsch, S., & Rumpf, S. (2006) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2006.11.005 · Cited by 280 · see citing works
Severson, A. F., Hamill, D. R., Carter, J. C., Schumacher, J. M., & Bowerman, B. A. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00715-6 · Cited by 236 · see citing works
Chromosome Alignment and Segregation Regulated by Ubiquitination of Survivin
Vong, Q. P., Cao, K., Li, H., Iglesias, P. A., & Zheng, Y. (2005) · Science · doi:10.1126/science.1120160 · Cited by 234 · see citing works
Audhya, A., Barron, F. E., McLeod, I. X., Maddox, A. S., Yates, J. R., Desai, A. B., & Oegema, K. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200506124 · Cited by 232 · see citing works
Kaitna, S., Pasierbek, P., Jantsch, M. F., Loidl, J., & Glotzer, M. (2002) · Current Biology · doi:10.1016/s0960-9822(02)00820-5 · Cited by 231 · see citing works
Remodelling the walls of the nucleus
Burke, B. E., & Ellenberg, J. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm860 · Cited by 225 · see citing works
Diverse functions with a common regulator: Ubiquitin takes command of an AAA ATPase
Ye, Y. (2006) · Journal of Structural Biology · doi:10.1016/j.jsb.2006.01.005 · Cited by 213 · see citing works
Kelly, A. E., Sampath, S. C., Maniar, T. A., Woo, E. M., Chait, B. T., & Funabiki, H. (2007) · Developmental Cell · doi:10.1016/j.devcel.2006.11.001 · Cited by 206 · see citing works
Aurora B controls the association of condensin I but not condensin II with mitotic chromosomes
Lipp, J., Hirota, T., Poser, I., & Peters, J. (2007) · Journal of Cell Science · doi:10.1242/jcs.03425 · Cited by 157 · see citing works
Wang, Y., Satoh, A., Warren, G., & Meyer, H. H. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200401010 · Cited by 154 · see citing works
Self-citationAurora-B associated protein phosphatases as negative regulators of kinase activation
Sugiyama, K., Sugiura, K., Hara, T., Sugimoto, K., Shima, H., Honda, K., Furukawa, K., Yamashita, S., & Urano, T. (2002) · Oncogene · doi:10.1038/sj.onc.1205432 · Cited by 150 · see citing works
Poteryaev, D. A., Squirrell, J. M., Campbell, J. M., White, J. G., & Spang, A. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-08-0726 · Cited by 140 · see citing works
Dynamic associations of heterochromatin protein 1 with the nuclear envelope
Kourmouli, N., Theodoropoulos, P. A., Dialynas, G., Bakou, A., Politou, A. S., Cowell, I. G., Singh, P. B., & Georgatos, S. D. (2000) · The EMBO Journal · doi:10.1093/emboj/19.23.6558 · Cited by 111 · see citing works
Analysis of the role of Aurora B on the chromosomal targeting of condensin I
Takemoto, A., Murayama, A., Katano, M., Urano, T., Furukawa, K., Yokoyama, S., Yanagisawa, J., Hanaoka, F., & Kimura, K. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm157 · Cited by 61 · see citing works
A conserved role of Caenorhabditis elegans CDC-48 in ER-associated protein degradation
Mouysset, J., Kähler, C., & Hoppe, T. (2006) · Journal of Structural Biology · doi:10.1016/j.jsb.2006.02.015 · Cited by 43 · see citing works
The nuclear envelope: filling in gaps
Burke, B. E. (2001) · Nature Cell Biology · doi:10.1038/ncb1201-e273 · Cited by 27 · see citing works
Chapter 17 Analysis of Nuclear Envelope Assembly Using Extracts of Xenopus Eggs
Lohka, M. J. (1997) · Methods in cell biology · doi:10.1016/s0091-679x(08)60887-0 · Cited by 24 · see citing works
Comparative analysis of expression of two p97 homologues in Caenorhabditis elegans
Yamauchi, S., Yamanaka, K., & Ogura, T. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.04.160 · Cited by 18 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis
Carmena, M., Wheelock, M., Funabiki, H., & Earnshaw, W. C. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3474 · Cited by 891 · see citing works
Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system
Meyer, H. H., Bug, M., & Bremer, S. (2012) · Nature Cell Biology · doi:10.1038/ncb2407 · Cited by 803 · see citing works
Self-citationCatastrophic nuclear envelope collapse in cancer cell micronuclei
Hatch, E. M., Fischer, A. H., Deerinck, T. J., & Hetzer, M. W. (2013) · Cell · doi:10.1016/j.cell.2013.06.007 · Cited by 741 · see citing works
Aggrephagy: Selective Disposal of Protein Aggregates by Macroautophagy
Lamark, T., & Johansen, T. (2012) · International Journal of Cell Biology · doi:10.1155/2012/736905 · Cited by 490 · see citing works
Survivin Reads Phosphorylated Histone H3 Threonine 3 to Activate the Mitotic Kinase Aurora B
Kelly, A. E., Ghenoiu, C., Xue, J. Z., Zierhut, C., Kimura, H., & Funabiki, H. (2010) · Science · doi:10.1126/science.1189505 · Cited by 466 · see citing works
Orchestrating nuclear envelope disassembly and reassembly during mitosis
Güttinger, S., Laurell, E., & Kutay, U. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2641 · Cited by 465 · see citing works
Tresse, E., Salomons, F. A., Vesa, J., Bott, L. C., Kimonis, V., Yao, T.-P., Dantuma, N. P., & Taylor, J. P. (2010) · Autophagy · doi:10.4161/auto.6.2.11014 · Cited by 437 · see citing works
The VCP/p97 system at a glance: connecting cellular function to disease pathogenesis
Meyer, H. H., & Weihl, C. C. (2014) · Journal of Cell Science · doi:10.1242/jcs.093831 · Cited by 423 · see citing works
Self-citationThe Aurora kinase family in cell division and cancer
Vader, G., & Lens, S. M. A. (2008) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2008.07.003 · Cited by 421 · see citing works
Sizing up the nucleus: nuclear shape, size and nuclear-envelope assembly
Webster, M. T., Witkin, K. L., & Cohen‐Fix, O. (2009) · Journal of Cell Science · doi:10.1242/jcs.037333 · Cited by 402 · see citing works
Mapping the Degradable Kinome Provides a Resource for Expedited Degrader Development
Donovan, K. A., Ferguson, F. M., Bushman, J. W., Eleuteri, N. A., Bhunia, D., Ryu, S., Tan, L., Shi, K., Yue, H., Liu, X., et al. (2020) · Cell · doi:10.1016/j.cell.2020.10.038 · Cited by 359 · see citing works
Mallette, F. A., Mattiroli, F., Cui, G., Young, L. C., Hendzel, M. J., Mer, G., Sixma, T. K., & Richard, S. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.47 · Cited by 358 · see citing works
ESCRT-III controls nuclear envelope reformation
Olmos, Y., Hodgson, L. R., Mantell, J., Verkade, P., & Carlton, J. G. (2015) · Nature · doi:10.1038/nature14503 · Cited by 355 · see citing works
Mechanisms and functions of nuclear envelope remodelling
Ungricht, R., & Kutay, U. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.153 · Cited by 343 · see citing works
Molecular control of animal cell cytokinesis
Fededa, J. P., & Gerlich, D. W. (2012) · Nature Cell Biology · doi:10.1038/ncb2482 · Cited by 331 · see citing works
Nuclear envelope assembly defects link mitotic errors to chromothripsis
Liu, S., Kwon, M., Mannino, M., Yang, N., Renda, F., Khodjakov, A., & Pellman, D. (2018) · Nature · doi:10.1038/s41586-018-0534-z · Cited by 314 · see citing works
The Nuclear EnvelopePreprint
Hetzer, M. W. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a000539 · Cited by 314 · see citing works
Molecular Mechanism of Substrate Processing by the Cdc48 ATPase Complex
Bodnar, N. O., & Rapoport, T. A. (2017) · Cell · doi:10.1016/j.cell.2017.04.020 · Cited by 312 · see citing works
Targeting the endoplasmic reticulum-stress response as an anticancer strategy
Healy, S., Gorman, A. M., Mousavi-Shafaei, P., Gupta, S., & Samali, A. (2009) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2009.06.064 · Cited by 305 · see citing works
Retrotranslocation of a Misfolded Luminal ER Protein by the Ubiquitin-Ligase Hrd1p
Carvalho, P., Stanley, A. M., & Rapoport, T. A. (2010) · Cell · doi:10.1016/j.cell.2010.10.028 · Cited by 297 · see citing works
Phosphatases: providing safe passage through mitotic exit
Wurzenberger, C., & Gerlich, D. W. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3149 · Cited by 293 · see citing works
The AAA-ATPase VCP/p97 promotes 53BP1 recruitment by removing L3MBTL1 from DNA double-strand breaks
Ács, K., Luijsterburg, M. S., Ackermann, L., Salomons, F. A., Hoppe, T., & Dantuma, N. P. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2188 · Cited by 280 · see citing works
UBX domain proteins: major regulators of the AAA ATPase Cdc48/p97
Schuberth, C. E., & Buchberger, A. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8072-8 · Cited by 277 · see citing works
Polyubiquitin chains: functions, structures, and mechanisms
Li, W., & Ye, Y. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8090-6 · Cited by 270 · see citing works
The ubiquitin-selective segregase VCP/p97 orchestrates the response to DNA double-strand breaks
Meerang, M., Ritz, D., Paliwal, S., Garajovà, Z., Bosshard, M., Mailand, N., Janščák, P., Hübscher, U., Meyer, H. H., & Ramadan, K. (2011) · Nature Cell Biology · doi:10.1038/ncb2367 · Cited by 258 · see citing works
Self-citationWeihl, C. C., Pestronk, A., & Kimonis, V. E. (2009) · Neuromuscular Disorders · doi:10.1016/j.nmd.2009.01.009 · Cited by 236 · see citing works
Cdc48: a power machine in protein degradation
Stolz, A., Hilt, W., Buchberger, A., & Wolf, D. H. (2011) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2011.06.001 · Cited by 226 · see citing works
Ritz, D., Vuk, M., Kirchner, P., Bug, M., Schütz, S., Hayer, A., Bremer, S., Lusk, C., Baloh, R. H., Lee, H., et al. (2011) · Nature Cell Biology · doi:10.1038/ncb2301 · Cited by 224 · see citing works
Self-citationErnst, R., Mueller, B., Ploegh, H. L., & Schlieker, C. D. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.09.016 · Cited by 222 · see citing works
Cdc48/p97 mediates UV-dependent turnover of RNA Pol II
Verma, R., Oania, R., Fang, R., Smith, G. T., & Deshaies, R. J. (2011) · Molecular Cell · doi:10.1016/j.molcel.2010.12.017 · Cited by 196 · see citing works
Recent advances in p97/VCP/Cdc48 cellular functions
Yamanaka, K., Sasagawa, Y., & Ogura, T. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.07.001 · Cited by 191 · see citing works
Besche, H. C., Haas, W., Gygi, S. P., & Goldberg, A. L. (2009) · Biochemistry · doi:10.1021/bi802198q · Cited by 183 · see citing works
A Mighty “Protein Extractor” of the Cell: Structure and Function of the p97/CDC48 ATPase
Ye, Y., Tang, W. K., Zhang, T., & Xia, D. (2017) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2017.00039 · Cited by 181 · see citing works
Deubiquitinases Maintain Protein Homeostasis and Survival of Cancer Cells upon Glutathione Depletion
Harris, I. S., Endress, J. E., Coloff, J. L., Selfors, L. M., McBrayer, S. K., Rosenbluth, J. M., Takahashi, N., Dhakal, S., Koduri, V., Oser, M. G., et al. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.01.020 · Cited by 168 · see citing works
The ubiquitin-dependent ATPase p97 removes cytotoxic trapped PARP1 from chromatin
Krastev, D. B., Li, S., Sun, Y., Wicks, A. J., Hoslett, G., Weekes, D. B., Badder, L. M., Knight, E. G., Marlow, R., Pardo, M., et al. (2022) · Nature Cell Biology · doi:10.1038/s41556-021-00807-6 · Cited by 163 · see citing works
Self-citationWang, Q., Shinkre, B. A., Lee, J., Weniger, M. A., Liu, Y., Chen, W., Wiestner, A. U., Trenkle, W. C., & Ye, Y. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015479 · Cited by 160 · see citing works
Structure and function of the AAA+ ATPase p97/Cdc48p
Xia, D., Tang, W. K., & Ye, Y. (2016) · Gene · doi:10.1016/j.gene.2016.02.042 · Cited by 159 · see citing works
Ku80 removal from DNA through double strand break–induced ubiquitylation
Postow, L., Ghenoiu, C., Woo, E. M., Krutchinsky, A. N., Chait, B. T., & Funabiki, H. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200802146 · Cited by 157 · see citing works
Chromosome condensation and decondensation during mitosis
Antonin, W., & Neumann, H. (2016) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2016.01.013 · Cited by 149 · see citing works
Golgi Structure and Function in Health, Stress, and Diseases
Li, J., Ahat, E., & Wang, Y. (2019) · Results and problems in cell differentiation · doi:10.1007/978-3-030-23173-6_19 · Cited by 146 · see citing works
Cell division control by the Chromosomal Passenger Complex
van der Waal, M. S., Hengeveld, R. C. C., van der Horst, A., & Lens, S. M. A. (2012) · Experimental Cell Research · doi:10.1016/j.yexcr.2012.03.015 · Cited by 145 · see citing works
Proteomic profiling of VCP substrates links VCP to K6‐linked ubiquitylation and c‐Myc function
Heidelberger, J. B., Voigt, A., Borisova, M. E., Petrosino, G., Ruf, S., Wagner, S., & Beli, P. (2018) · EMBO Reports · doi:10.15252/embr.201744754 · Cited by 138 · see citing works
Maerki, S., Olma, M. H., Staubli, T., Steigemann, P., Gerlich, D. W., Quadroni, M., Sumara, I., & Peter, M. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200906117 · Cited by 133 · see citing works
Finding the will and the way of ERAD substrate retrotranslocation
Hampton, R. Y., & Sommer, T. (2012) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2012.05.010 · Cited by 133 · see citing works
Role of Cdc48/p97 as a SUMO-targeted segregase curbing Rad51–Rad52 interaction
Bergink, S., Ammon, T., Kern, M. J., Schermelleh, L., Leonhardt, H., & Jentsch, S. (2013) · Nature Cell Biology · doi:10.1038/ncb2729 · Cited by 130 · see citing works
Puumalainen, M.-R., Lessel, D., Rüthemann, P., Kaczmarek, N., Bachmann, K., Ramadan, K., & Naegeli, H. (2014) · Nature Communications · doi:10.1038/ncomms4695 · Cited by 129 · see citing works
Self-citationRanBP2 and SENP3 Function in a Mitotic SUMO2/3 Conjugation-Deconjugation Cycle on Borealin
Klein, U. R., Haindl, M., Nigg, E. A., & Müller, S. P. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-05-0511 · Cited by 127 · see citing works
Nuclear pore complex assembly through the cell cycle: Regulation and membrane organization
Antonin, W., Ellenberg, J., & Dultz, E. (2008) · FEBS Letters · doi:10.1016/j.febslet.2008.02.067 · Cited by 127 · see citing works
Cell division: control of the chromosomal passenger complex in time and space
van der Horst, A., & Lens, S. M. A. (2013) · Chromosoma · doi:10.1007/s00412-013-0437-6 · Cited by 124 · see citing works
Lysine methylation of VCP by a member of a novel human protein methyltransferase family
Kernstock, S., Davydova, E., Jakobsson, M. E., Moen, A. R., Pettersen, S., Mælandsmo, G. M., Egge-Jacobsen, W. M., & Falnes, P. Ø. (2012) · Nature Communications · doi:10.1038/ncomms2041 · Cited by 124 · see citing works
Reorganization of the nuclear envelope during open mitosis
Kutay, U., & Hetzer, M. W. (2008) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2008.09.010 · Cited by 123 · see citing works
Feedback control of chromosome separation by a midzone Aurora B gradient
Afonso, O., Matos, I., Pereira, A. J., Aguiar, P., Lampson, M. A., & Maiato, H. (2014) · Science · doi:10.1126/science.1251121 · Cited by 122 · see citing works
A Conserved Unfoldase Activity for the p97 AAA-ATPase in Proteasomal Degradation
Beskow, A., Grimberg, K. B., Bott, L. C., Salomons, F. A., Dantuma, N. P., & Young, P. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.09.050 · Cited by 115 · see citing works
Emerging regulatory mechanisms in ubiquitin-dependent cell cycle control
Mocciaro, A., & Rapé, M. (2012) · Journal of Cell Science · doi:10.1242/jcs.091199 · Cited by 110 · see citing works
Liu, Y., & Ye, Y. (2011) · Cell Research · doi:10.1038/cr.2011.75 · Cited by 110 · see citing works
Raman, M., Havens, C. G., Walter, J. C., & Harper, J. W. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.06.036 · Cited by 108 · see citing works
TRIM 21: a cytosolic Fc receptor with broad antibody isotype specificity
Foss, S., Watkinson, R., Sandlie, I., James, L. C., & Andersen, J. T. (2015) · Immunological Reviews · doi:10.1111/imr.12363 · Cited by 108 · see citing works
Nucleosomal regulation of chromatin composition and nuclear assembly revealed by histone depletion
Zierhut, C., Jenness, C., Kimurâ, H., & Funabiki, H. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2845 · Cited by 106 · see citing works
Structure, Dynamics and Function of the 26S Proteasome
Mao, Y. (2020) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-3-030-58971-4_1 · Cited by 105 · see citing works
Kitagawa, M., & Lee, S. H. (2015) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2015.00014 · Cited by 104 · see citing works
Growing sphere of influence: Cdc48/p97 orchestrates ubiquitin-dependent extraction from chromatin
Dantuma, N. P., & Hoppe, T. (2012) · Trends in Cell Biology · doi:10.1016/j.tcb.2012.06.003 · Cited by 101 · see citing works
AAA ATPase p97/VCP is essential for TRIM21-mediated virus neutralization
Hauler, F., Mallery, D. L., McEwan, W. A., Bidgood, S. R., & James, L. C. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210659109 · Cited by 101 · see citing works
Critical Role of VCP/p97 in the Pathogenesis and Progression of Non-Small Cell Lung Carcinoma
Valle, C. W., Min, T., Bodas, M., Mazur, S., Begum, S., Tang, D., & Vij, N. (2011) · PLoS ONE · doi:10.1371/journal.pone.0029073 · Cited by 101 · see citing works
Altered cofactor regulation with disease-associated p97/VCP mutations
Zhang, X., Gui, L., Zhang, X., Bulfer, S. L., Sanghez, V., Wong, D., Lee, Y., Lehmann, L. W., Lee, J. S., Shih, P.-Y., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1418820112 · Cited by 99 · see citing works
The ESCRT machinery: new roles at new holes
Olmos, Y., & Carlton, J. (2016) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2015.12.001 · Cited by 98 · see citing works
The p97 ATPase associates with EEA1 to regulate the size of early endosomes
Ramanathan, H. N., & Ye, Y. (2011) · Cell Research · doi:10.1038/cr.2011.80 · Cited by 98 · see citing works
Growing functions of the ESCRT machinery in cell biology and viral replication
Scourfield, E. J., & Martin‐Serrano, J. (2017) · Biochemical Society Transactions · doi:10.1042/bst20160479 · Cited by 92 · see citing works
Role of p97/VCP (Cdc48) in genome stability
Vaz, B., Halder, S., & Ramadan, K. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00060 · Cited by 91 · see citing works
Self-citationValosin-Containing Protein (VCP)/p97: A Prognostic Biomarker and Therapeutic Target in Cancer
Costantini, S., Capone, F., Polo, A., Bagnara, P., & Budillon, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221810177 · Cited by 88 · see citing works
Nie, M., Aslanian, A., Prudden, J., Heideker, J., Vashisht, A. A., Wohlschlegel, J. A., Yates, J. R., & Boddy, M. N. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.379768 · Cited by 87 · see citing works
Dynamic ubiquitin signaling in cell cycle regulation
Gilberto, S., & Peter, M. (2017) · The Journal of Cell Biology · doi:10.1083/jcb.201703170 · Cited by 86 · see citing works
The p97/VCP ATPase is critical in muscle atrophy and the accelerated degradation of muscle proteins
Piccirillo, R., & Goldberg, A. L. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.178 · Cited by 85 · see citing works
Ring of Change: CDC48/p97 Drives Protein Dynamics at Chromatin
Franz, A., Ackermann, L., & Hoppe, T. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00073 · Cited by 84 · see citing works
The Abscission Checkpoint: Making It to the Final Cut
Nähse, V., Christ, L., Stenmark, H., & Campsteijn, C. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2016.10.001 · Cited by 83 · see citing works
Mérai, Z., Chumak, N., García-Aguilar, M., Hsieh, T., Nishimura, T., Schoft, V. K., Bindics, J., Ślusarz, L., Arnoux, S., Opravil, S., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1418564111 · Cited by 83 · see citing works
Nuclear Reformation at the End of Mitosis
Schellhaus, A. K., Magistris, P. D., & Antonin, W. (2015) · Journal of Molecular Biology · doi:10.1016/j.jmb.2015.09.016 · Cited by 82 · see citing works
Chen, M., Gutierrez, G. J., & Ronai, Z. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100028108 · Cited by 82 · see citing works
Cell cycle progression requires the CDC-48 UFD−1/NPL−4 complex for efficient DNA replication
Mouysset, J., Deichsel, A., Moser, S. C., Hoege, C., Hyman, A. A., Gartner, A., & Hoppe, T. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805944105 · Cited by 82 · see citing works
Wurzenberger, C., Held, M., Lampson, M. A., Poser, I., Hyman, A. A., & Gerlich, D. W. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201112112 · Cited by 81 · see citing works
Schooley, A., Vollmer, B., & Antonin, W. (2012) · Chromosoma · doi:10.1007/s00412-012-0388-3 · Cited by 79 · see citing works
K29-linked ubiquitin signaling regulates proteotoxic stress response and cell cycle
Yu, Y., Zheng, Q., Erramilli, S. K., Pan, M., Park, S.-J., Xie, Y., Li, J., Fei, J., Kossiakoff, A. A., Liu, L., et al. (2021) · Nature Chemical Biology · doi:10.1038/s41589-021-00823-5 · Cited by 78 · see citing works
Inhibitors of the ATPase p97/VCP: From basic research to clinical applications
Kilgas, S., & Ramadan, K. (2023) · Cell chemical biology · doi:10.1016/j.chembiol.2022.12.007 · Cited by 78 · see citing works
Self-citationDargemont, C., & Ossareh‐Nazari, B. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.07.011 · Cited by 76 · see citing works
Platani, M., Santarella‐Mellwig, R., Posch, M., Walczak, R., Swedlow, J. R., & Mattaj, I. W. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-05-0377 · Cited by 76 · see citing works
Neuronal remodeling and apoptosis require VCP-dependent degradation of the apoptosis inhibitor DIAP1
Rumpf, S., Lee, S. B., Jan, L. Y., & Jan, Y. N. (2011) · Development · doi:10.1242/dev.062703 · Cited by 74 · see citing works
New ATPase regulators—p97 goes to the PUB
Madsen, L., Seeger, M., Semple, C. A. M., & Hartmann‐Petersen, R. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.05.017 · Cited by 72 · see citing works
SUMOylation modulates the function of Aurora-B kinase
Fernández‐Miranda, G., de Castro, I. P., Carmena, M., Aguirre‐Portolés, C., Ruchaud, S., Fant, X., Montoya, G., Earnshaw, W. C., & Malumbres, M. (2010) · Journal of Cell Science · doi:10.1242/jcs.065565 · Cited by 72 · see citing works
Novel ESCRT functions in cell biology: spiraling out of control?
Campsteijn, C., Vietri, M., & Stenmark, H. (2016) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2016.03.008 · Cited by 71 · see citing works
Ubiquitin-Mediated Degradation of Aurora Kinases
Lindon, C., Grant, R., & Min, M. (2016) · Frontiers in Oncology · doi:10.3389/fonc.2015.00307 · Cited by 71 · see citing works
Fujita, K., Nakamura, Y., Oka, T., Ito, H., Tamura, T., Tagawa, K., Sasabe, T., Katsuta, A., Motoki, K., Shiwaku, H., et al. (2013) · Nature Communications · doi:10.1038/ncomms2828 · Cited by 69 · see citing works
Bin, B., Hojyo, S., Hosaka, T., Bhin, J., Kano, H., Miyai, T., Ikeda, M., Kimura‐Someya, T., Shirouzu, M., Cho, E., et al. (2014) · EMBO Molecular Medicine · doi:10.15252/emmm.201303809 · Cited by 68 · see citing works
Arita, M., Wakita, T., & Shimizu, H. (2012) · Journal of Virology · doi:10.1128/jvi.00114-12 · Cited by 67 · see citing works
The coordination of nuclear envelope assembly and chromosome segregation in metazoans
Liu, S., & Pellman, D. S. (2020) · Nucleus · doi:10.1080/19491034.2020.1742064 · Cited by 67 · see citing works
Wilcox, A. J., & Laney, J. D. (2009) · Nature Cell Biology · doi:10.1038/ncb1997 · Cited by 66 · see citing works
Importin β Regulates the Seeding of Chromatin with Initiation Sites for Nuclear Pore Assembly
Rotem, A., Gruber, R., Shorer, H., Shaulov, L., Klein, E., & Harel, A. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-02-0150 · Cited by 66 · see citing works
KLHL41 stabilizes skeletal muscle sarcomeres by nonproteolytic ubiquitination
Ramirez-Martinez, A., Cenik, B. K., Bezprozvannaya, S., Chen, B., Bassel‐Duby, R., Liu, N., & Olson, E. N. (2017) · eLife · doi:10.7554/elife.26439 · Cited by 66 · see citing works
Pelisch, F., Sonneville, R., Pourkarimi, E., Agostinho, A., Blow, J. J., Gartner, A., & Hay, R. T. (2014) · Nature Communications · doi:10.1038/ncomms6485 · Cited by 65 · see citing works
Chromatin-Bound Xenopus Dppa2 Shapes the Nucleus by Locally Inhibiting Microtubule Assembly
Xue, J. Z., Woo, E. M., Postow, L., Chait, B. T., & Funabiki, H. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.08.002 · Cited by 63 · see citing works
The p97–UBXD8 complex destabilizes mRNA by promoting release of ubiquitinated HuR from mRNPPreprint
Zhou, H.-L., Geng, C., Luo, G., & Lou, H. J. (2013) · Genes & Development · doi:10.1101/gad.215681.113 · Cited by 62 · see citing works
Role of autophagy in muscle disease
Franco‐Romero, A., & Sandri, M. (2021) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2021.101041 · Cited by 61 · see citing works
- Authors
- Ramadan, K., Bruderer, R., Spiga, F. M., Popp, O., Baur, T., Gotta, M., & Meyer, H. H.
- Affiliations
- ETH Zurich (CH)
- University of Geneva (CH)
- Corresponding author
- Meyer, Hemmo H.
- Venue
- Nature
- Published
- 2007-12
- Volume
- 450
- Issue
- 7173
- Pages
- 1258-1262
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1981835453
- Cited by
- 261
- References
- 33
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 7 · 2023: 10 · 2022: 13 · 2021: 7 · 2020: 16 · 2019: 8 · 2018: 8 · 2017: 16 · 2016: 15 · 2015: 13 · 2014: 20 · 2013: 17 · 2012: 29
- FWCI
- 6.09
- Type
- journal article
- Language
- en
- Open access
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Keywords
- Cdc48/p97, Aurora B kinase, nuclear envelope reformation, mitosis, chromatin decondensation, ubiquitination, AAA+ ATPase, nuclear envelope assembly, chromosome segregation
- MeSH terms
- Valosin Containing Protein, Adenosine Triphosphatases, Animals, Cell Nucleus, Chromatin, Female, Male, Nuclear Envelope, Xenopus laevis, Caenorhabditis elegans, Protein Serine-Threonine Kinases, Cell Cycle Proteins, Ubiquitin, RNA Interference, Ubiquitination, Aurora Kinases
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review