Requirement of Hsp90 for centrosomal function reflects its regulation of Polo kinase stability
Open accessAbstract
We have previously shown that the molecular chaperone heat shock protein 90 (Hsp90) is required to ensure proper centrosome function in Drosophila and vertebrate cells. This observation led to the hypothesis that this chaperone could be required for the stability of one or more centrosomal proteins. We have found that one of these is Polo, a protein kinase known to regulate several aspects of cell division including centrosome maturation and function. Inhibition of Hsp90 results in the inactivation of Polo kinase activity. It also leads to a loss in the ability of cytoplasmic extracts to complement the failure of salt-stripped preparations of centrosomes to nucleate microtubules. This effect can be rescued upon addition of active recombinant POLO: We also show that Polo and Hsp90 are part of a complex and conclude that stabilization of Polo is one of the mechanisms by which Hsp90 contributes to the maintenance of functional centrosomes.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Several key regulators of cell cycle progression have been implicated as Hsp90 interactors, including the mammalian tyrosine kinase Wee1 and its budding yeast homologue Swe1, the polo-like kinase Plk1 and its yeast homologue Cdc5, and the cyclin-dependent kinase Cdc2 and its budding yeast homologue Cdc28.
“Several key regulators of cell cycle progression have been implicated as Hsp90 interactors, including the mammalian tyrosine kinase Wee1 and its budding yeast homologue Swe1, the polo-like kinase Plk1 and its yeast homologue Cdc5, and the cyclin-dependent kinase Cdc2 and its budding yeast homologue Cdc28 (Aligue et al., 1994; Munoz and Jimenez, 1999; de Carcer et al., 2001; Goes and Martin, 2001;”
From Cdc28 provides a molecular link between Hsp90, morphogenesis, and cell cycle progression in<i>Candida albicans</i> (2012) · cites this paper as de Carcer et al., 2001
Plk1, the mammalian homologue of Cdc5, is an Hsp90 client protein, and Cdc5 interacts with an Hsp90 cochaperone, Cdc37, in S. cerevisiae.
“This is intriguing, as Plk1, the mammalian homologue of Cdc5, is an Hsp90 client protein, and Cdc5 interacts with an Hsp90 cochaperone, Cdc37, in S. cerevisiae (de Carcer et al., 2001; de Carcer, 2004; Mort-Bontemps-Soret et al., 2002).”
From Cdc28 provides a molecular link between Hsp90, morphogenesis, and cell cycle progression in<i>Candida albicans</i> (2012) · cites this paper as de Carcer et al., 2001
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Parsell, D. A., & Lindquist, S. (1993) · Annual Review of Genetics · doi:10.1146/annurev.ge.27.120193.002253 · Cited by 2,275 · see citing works
Steroid Receptor Interactions with Heat Shock Protein and Immunophilin Chaperones*
Pratt, W. B., & Toft, D. O. (1997) · Endocrine Reviews · doi:10.1210/edrv.18.3.0303 · Cited by 1,791 · see citing works
Stebbins, C. E., Russo, A. A., Schneider, C. B., Rosen, N. X., Hartl, F. U., & Pavletich, N. P. (1997) · Cell · doi:10.1016/s0092-8674(00)80203-2 · Cited by 1,370 · see citing works
Prodromou, C., Roe, S. M., O’Brien, R., Ladbury, J. E., Piper, P. W., & Pearl, L. H. (1997) · Cell · doi:10.1016/s0092-8674(00)80314-1 · Cited by 1,258 · see citing works
Zou, J., Guo, Y., Guettouche, T., Smith, D. F., & Voellmy, R. W. (1998) · Cell · doi:10.1016/s0092-8674(00)81588-3 · Cited by 1,232 · see citing works
Dynamic activation of endothelial nitric oxide synthase by Hsp90
García‐Cardeña, G., Fan, R., Shah, V. H., Sorrentino, R., Cirino, G., Papapetropoulos, A., & Sessa, W. C. (1998) · Nature · doi:10.1038/33934 · Cited by 1,029 · see citing works
ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo
Panaretou, B., Prodromou, C., Roe, S. M., O'Brien, R., Ladbury, J. E., Piper, P. W., & Pearl, L. H. (1998) · The EMBO Journal · doi:10.1093/emboj/17.16.4829 · Cited by 735 · see citing works
Lane, H. A., & Nigg, E. A. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.135.6.1701 · Cited by 695 · see citing works
Steroid Receptor Interactions with Heat Shock Protein and Immunophilin Chaperones
Pratt, W. B. (1997) · Endocrine Reviews · doi:10.1210/er.18.3.306 · Cited by 641 · see citing works
Hsp90 & Co. – a holding for folding
Büchner, J. (1999) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(99)01373-0 · Cited by 625 · see citing works
Polo, a mitotic mutant of Drosophila displaying abnormal spindle poles
Sunkel, C. E., & Glover, D. M. (1988) · Journal of Cell Science · doi:10.1242/jcs.89.1.25 · Cited by 563 · see citing works
Self-citationFunctional requirement of p23 and Hsp90 in telomerase complexesPreprint
Holt, S. E., Aisner, D. L., Baur, J. A., Tesmer, V. M., Dy, M., Ouellette, M., Trager, J. B., Morin, G. B., Toft, D. O., Shay, J. W., et al. (1999) · Genes & Development · doi:10.1101/gad.13.7.817 · Cited by 533 · see citing works
Polo-like kinases: a team that plays throughout mitosisPreprint
Glover, D. M., Hagan, I., & Tavares, Á. A. (1998) · Genes & Development · doi:10.1101/gad.12.24.3777 · Cited by 427 · see citing works
Self-citationMutational Analysis of Hsp90 Function: Interactions with a Steroid Receptor and a Protein Kinase
Nathan, D. F., & Lindquist, S. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.7.3917 · Cited by 423 · see citing works
polo encodes a protein kinase homolog required for mitosis in Drosophila.Preprint
Llamazares, S., Moreira, A., Tavares, Á. A., Girdham, C. H., Spruce, B. A., González, C., Karess, R. E., Glover, D. M., & Sunkel, C. E. (1991) · Genes & Development · doi:10.1101/gad.5.12a.2153 · Cited by 400 · see citing works
Self-citationLoo, M. A., Jensen, T. J., Cui, L., Hou, Y.-X., Chang, X.-B., & Riordan, J. R. (1998) · The EMBO Journal · doi:10.1093/emboj/17.23.6879 · Cited by 374 · see citing works
Ohkura, H., Hagan, I., & Glover, D. M. (1995) · Genes & Development · doi:10.1101/gad.9.9.1059 · Cited by 372 · see citing works
Self-citation<i>In vivo</i> functions of the <i>Saccharomyces cerevisiae</i> Hsp90 chaperone
Nathan, D. F., Vos, M. H., & Lindquist, S. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.24.12949 · Cited by 364 · see citing works
Polo-like kinases: positive regulators of cell division from start to finish
Nigg, E. A. (1998) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(98)80121-x · Cited by 344 · see citing works
Pratt, W. B. (1997) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.37.1.297 · Cited by 333 · see citing works
Kotani, S., Tugendreich, S., Fujii, M., Jorgensen, P.-M., Watanabe, N., Höög, C., Hieter, P., & Todokoro, K. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80037-4 · Cited by 301 · see citing works
Cutforth, T. (1994) · Cell · doi:10.1016/0092-8674(94)90442-1 · Cited by 287 · see citing works
Aligue, R., Akhavan‐Niak, H., & Russell, P. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06956.x · Cited by 261 · see citing works
Salisbury, J. L., Baron, A. T., & Sanders, M. A. (1988) · The Journal of Cell Biology · doi:10.1083/jcb.107.2.635 · Cited by 245 · see citing works
Activated Polo-Like Kinase Plx1 Is Required at Multiple Points during Mitosis in Xenopus laevis
Qian, Y., ERIKSON, E., Li, C., & Maller, J. L. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.7.4262 · Cited by 238 · see citing works
Recruitment of the γ-Tubulin Ring Complex to Drosophila Salt-stripped Centrosome Scaffolds
Moritz, M., Zheng, Y., Alberts, B., et al. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.3.775 · Cited by 226 · see citing works
Three-dimensional structural characterization of centrosomes from early Drosophila embryos.
Moritz, M., Braunfeld, M. B., Fung, J. C., et al. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.130.5.1149 · Cited by 209 · see citing works
Gergely, F. V., Kidd, D., Jeffers, K., Wakefield, J. G., & Raff, J. W. (2000) · The EMBO Journal · doi:10.1093/emboj/19.2.241 · Cited by 195 · see citing works
Avides, M. D. C., & Glover, D. M. (1999) · Science · doi:10.1126/science.283.5408.1733 · Cited by 169 · see citing works
Self-citationPuca, G. A., Nola, E., Sica, V., et al. (1972) · Biochemistry · doi:10.1021/bi00772a020 · Cited by 157 · see citing works
Saunders, R. D. C., Avides, M. D. C., Howard, T., González, C., & Glover, D. M. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.137.4.881 · Cited by 147 · see citing works
Self-citationTestosterone Cytosol “Receptor” in the Rat Levator Ani Muscle
Jung, I., & Baulieu, É.-É. (1972) · Nature New Biology · doi:10.1038/newbio237024a0 · Cited by 142 · see citing works
Cloning of a gene encoding an antigen associated with the centrosome in Drosophila
Whitfield, W. G. F., Millar, S. E., Saumweber, H., Frasch, M., & Glover, D. M. (1988) · Journal of Cell Science · doi:10.1242/jcs.89.4.467 · Cited by 141 · see citing works
Self-citationThe heat shock protein 83 (Hsp83) is required for Raf‐mediated signalling in Drosophila
van der Straten, A., Rommel, C., Dickson, B. J., & Hafen, E. (1997) · The EMBO Journal · doi:10.1093/emboj/16.8.1961 · Cited by 140 · see citing works
Parsell, D. (1993) · Annual Review of Genetics · doi:10.1146/annurev.genet.27.1.437 · Cited by 140 · see citing works
The Homeotic Target Gene centrosomin Encodes an Essential Centrosomal Component
Li, K., & Kaufman, T. C. (1996) · Cell · doi:10.1016/s0092-8674(00)81258-1 · Cited by 127 · see citing works
Polo kinase and Asp are needed to promote the mitotic organizing activity of centrosomes
Avides, M. D. C., Tavares, Á. A., & Glover, D. M. (2001) · Nature Cell Biology · doi:10.1038/35070110 · Cited by 126 · see citing works
Self-citationLange, B. M. H., Bachi, A., Wilm, M., & González, C. (2000) · The EMBO Journal · doi:10.1093/emboj/19.6.1252 · Cited by 123 · see citing works
Self-citationHelps, N. R., Brewis, N., Lineruth, K., et al. (1998) · Journal of Cell Science · doi:10.1242/jcs.111.10.1331 · Cited by 123 · see citing works
Genetic Analysis of Viable Hsp90 Alleles Reveals a Critical Role in Drosophila Spermatogenesis
Yue, L., Karr, T. L., Nathan, D. F., Swift, H., Srinivasan, S., & Lindquist, S. L. (1999) · Genetics · doi:10.1093/genetics/151.3.1065 · Cited by 122 · see citing works
Mutations in the Plk gene lead to instability of Plk protein in human tumour cell lines
Simizu, S., & Osada, H. (2000) · Nature Cell Biology · doi:10.1038/35041102 · Cited by 120 · see citing works
Barnett, C. A., Schmidt, T. J., & Litwack, G. (1980) · Biochemistry · doi:10.1021/bi00564a046 · Cited by 115 · see citing works
Logarinho, E., & Sunkel, C. E. (1998) · Journal of Cell Science · doi:10.1242/jcs.111.19.2897 · Cited by 103 · see citing works
Essential role for γ‐tubulin in the acentriolar female meiotic spindle of Drosophila
Tavosanis, G., Llamazares, S., Goulielmos, G., et al. (1997) · The EMBO Journal · doi:10.1093/emboj/16.8.1809 · Cited by 99 · see citing works
Kellogg, D. R., Oegema, K., Raff, J. W., et al. (1995) · Molecular Biology of the Cell · doi:10.1091/mbc.6.12.1673 · Cited by 56 · see citing works
ATP-dependent activation of glucocorticoid receptor from rat liver cytosol
Moudgil, V. K., & John, J. (1980) · Biochemical Journal · doi:10.1042/bj1900799 · Cited by 53 · see citing works
Muñoz, M. J., & Jiménez, J. (1999) · Molecular and General Genetics MGG · doi:10.1007/s004380050963 · Cited by 52 · see citing works
Riparbelli, M. G., Callaini, G., & Glover, D. M. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.18.3341 · Cited by 51 · see citing works
Self-citationLK6, a short lived protein kinase in Drosophila that can associate with microtubules and centrosomes
Kidd, D., & Raff, J. W. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.2.209 · Cited by 39 · see citing works
The response of the centrosome to heat shock and related stresses in a Drosophila cell line
Debec, A., Courgeon, A., Maingourd, M., et al. (1990) · Journal of Cell Science · doi:10.1242/jcs.96.3.403 · Cited by 36 · see citing works
González, C., Sunkel, C. E., & Glover, D. M. (1998) · Chromosoma · doi:10.1007/s004120050329 · Cited by 33 · see citing works
Self-citationIn Vitro Stabilization of the Unoccupied Glucocorticoid Receptor by Adenosine 5'-Diphosphate*
Barnett, C. A., Palmour, R. M., Litwack, G., & Seegmiller, J. E. (1983) · Endocrinology · doi:10.1210/endo-112-6-2059 · Cited by 29 · see citing works
Holbrook, N. J., Bodwell, J. E., & Munck, A. U. (1983) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)43747-1 · Cited by 28 · see citing works
Chapter 1 Isolation of Centrosomes from Drosophila Embryos
Moritz, M., & Alberts, B. (1998) · Methods in cell biology · doi:10.1016/s0091-679x(08)61972-x · Cited by 22 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
HSP90 as a new therapeutic target for cancer therapy: the story unfolds
Maloney, A., & Workman, P. (2002) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2.1.3 · Cited by 531 · see citing works
Senn, H., Shapiro, R. S., & Cowen, L. E. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-08-0729 · Cited by 67 · see citing works
de Cárcer, G. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-2214 · Cited by 66 · see citing works
Wang, H., Zou, X., Wei, Z., Wu, Y., Li, R., Zeng, R., Chen, Z., & Liao, K. (2014) · Journal of Cell Science · doi:10.1242/jcs.155101 · Cited by 21 · see citing works
- Authors
- de Cárcer, G., do Carmo Avides, M., Lallena, M. J., Glover, D. M., & González, C.
- Affiliations
- European Molecular Biology Laboratory (DE)
- University of Cambridge (GB)
- Corresponding author
- González, Cayetano
- ORCID
- Glover, David M.
- Venue
- The EMBO Journal
- Published
- 2001-06-01
- Volume
- 20
- Issue
- 11
- Pages
- 2878-2884
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC125474
- OpenAlex
- W2168824053
- Cited by
- 90
- References
- 54
- Citations by year
- 2023: 1 · 2021: 2 · 2019: 5 · 2018: 2 · 2017: 3 · 2016: 3 · 2015: 2 · 2014: 4 · 2013: 2 · 2012: 2
- FWCI
- 2.27
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The EMBO Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- HSP90, Polo kinase, centrosome function, protein stability, molecular chaperones, centrosome maturation, microtubule nucleation, cell division regulation, kinase activity, protein complexes
- MeSH terms
- Animals, Cell Division, Cell Line, Drosophila melanogaster, Embryo, Nonmammalian, Genetic Complementation Test, Recombinant Proteins, Vertebrates, Protein Serine-Threonine Kinases, Centrosome, HSP90 Heat-Shock Proteins, Drosophila Proteins
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
