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Hsp90 as a capacitor for morphological evolution
Abstract
The heat-shock protein Hsp90 supports diverse but specific signal transducers and lies at the interface of several developmental pathways. We report here that when Drosophila Hsp90 is mutant or pharmacologically impaired, phenotypic variation affecting nearly any adult structure is produced, with specific variants depending on the genetic background and occurring both in laboratory strains and in wild populations. Multiple, previously silent, genetic determinants produced these variants and, when enriched by selection, they rapidly became independent of the Hsp90 mutation. Therefore, widespread variation affecting morphogenic pathways exists in nature, but is usually silent; Hsp90 buffers this variation, allowing it to accumulate under neutral conditions. When Hsp90 buffering is compromised, for example by temperature, cryptic variants are expressed and selection can lead to the continued expression of these traits, even when Hsp90 function is restored. This provides a plausible mechanism for promoting evolutionary change in otherwise entrenched developmental processes.
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“Hence Hsp90 has acted as an evolutionary capacitor during eukaryotic evolution19-21.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [19]
In the citing paper
“First, Hsp90 can buffer the effects of genetic or epigenetic variation, keeping it silent until released when the chaperone reservoir is compromised in response to stress.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [19]
In the citing paper
“This role as a capacitor for variation has been observed in diverse eukaryotes including flies, plants, and fungi18,19,129-134.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [19]
Citations
Cites
Introduction to Quantitative Genetics.
Edwards, A. W. F., & Falconer, D. S. (1982) · Biometrics · doi:10.2307/2529912 · Cited by 21,447
The Neutral Theory of Molecular Evolution
Kimura, M. (1979) · Scientific American · doi:10.1038/scientificamerican1179-98 · Cited by 7,687
The origins of order; self organization and selection in evolution
Kauffman, S. A. (1994) · International Journal of Biochemistry · doi:10.1016/0020-711x(94)90119-8 · Cited by 6,753
The Neutral Theory of Molecular Evolution
Kimura, M. (1983) · Cambridge University Press eBooks · doi:10.1017/cbo9780511623486 · Cited by 6,300
CANALIZATION OF DEVELOPMENT AND THE INHERITANCE OF ACQUIRED CHARACTERS
WADDINGTON, C. H. (1942) · Nature · doi:10.1038/150563a0 · Cited by 3,255
The Genome of Drosophila Melanogaster
Lindsley, D. L., & Zimm, G. G. (1992) · Cited by 3,098
GENETIC ASSIMILATION OF AN ACQUIRED CHARACTER
Waddington, C. H. (1953) · Evolution · doi:10.1111/j.1558-5646.1953.tb00070.x · Cited by 1,494
Whitesell, L., Mimnaugh, E. G., De Costa, B., Myers, C. E., & Neckers, L. M. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.18.8324 · Cited by 1,444
Raff, R. A. (1996) · University of Chicago Press eBooks · doi:10.7208/chicago/9780226256573.001.0001 · Cited by 1,262
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
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- Xu, Y., Singer, M. & Lindquist, S. Maturation of c-src as a kinase and as a substrate is dependent on Hsp90. Proc. Natl Acad. Sci. USA (in the press).
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Sorted by citations
Items 401–500 of 1,003
Shonhai, A., Maier, A., Przyborski, J., & Blatch, G. (2011) · Protein Peptide Letters · doi:10.2174/092986611794475002 · Cited by 109
Transposons, environmental changes, and heritable induced phenotypic variability
Piacentini, L., Fanti, L., Specchia, V., Bozzetti, M. P., Berloco, M. F., Palumbo, G., & Pimpinelli, S. (2014) · Chromosoma · doi:10.1007/s00412-014-0464-y · Cited by 118
Cagiada, M., Johansson, K. E., Valančiūtė, A., Nielsen, S. V., Hartmann‐Petersen, R., Yang, J. J. J., Fowler, D. M., Stein, A., & Lindorff‐Larsen, K. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab095 · Cited by 113
Lu, X., Xiao, L., Wang, L., & Ruden, D. M. (2011) · Biochemical Pharmacology · doi:10.1016/j.bcp.2011.11.011 · Cited by 118
The Opportunity for Canalization and the Evolution of Genetic Networks
Proulx, S. R., & Phillips, P. C. (2005) · The American Naturalist · doi:10.1086/426873 · Cited by 114
Diezmann, S., Michaut, M., Shapiro, R. S., Bader, G. D., & Cowen, L. E. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002562 · Cited by 112
Opposing effects of folding and assembly chaperones on evolvability of Rubisco
Durão, P., Aigner, H., Nagy, P., Mueller‐Cajar, O., Hartl, F. U., & Hayer-Hartl, M. K. (2015) · Nature Chemical Biology · doi:10.1038/nchembio.1715 · Cited by 112
A mother’s sacrifice: what is she keeping for herself?
Henderson, K. A., & Gottschling, D. E. (2008) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2008.09.004 · Cited by 117
Eggert, H., Kurtz, J., & de Buhr, M. F. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.2089 · Cited by 115
Redundancy, Feedback, and Robustness in the Arabidopsis thaliana BZR/BEH Gene Family
Lachowiec, J., Mason, G. A., Schultz, K., & Queitsch, C. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00523 · Cited by 112
Milton, C. C., Huynh, B., Batterham, P., Rutherford, S. L., & Hoffmann, A. A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1835613100 · Cited by 112
Self-citationGenes: Philosophical analyses put to the test
Stotz, K. C., & Griffiths, P. E. (2004) · History & Philosophy of the Life Sciences · doi:10.1080/03919710412331341621 · Cited by 111
Gidalevitz, T., Kikis, E. A., & Morimoto, R. I. (2010) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2009.11.001 · Cited by 114
Phenotypic plasticity, global change, and the speed of adaptive evolution
Gibert, P., Debat, V., & Ghalambor, C. K. (2019) · Current Opinion in Insect Science · doi:10.1016/j.cois.2019.06.007 · Cited by 110
Dawson, M. N., & Martin, L. E. (2001) · Springer eBooks · doi:10.1007/978-94-010-0722-1_21 · Cited by 110
Cellular Proteomes Have Broad Distributions of Protein Stability
Ghosh, K., & Dill, K. A. (2010) · Biophysical Journal · doi:10.1016/j.bpj.2010.10.036 · Cited by 115
&cestflwr; The Hsp90 family of proteins in Arabidopsis thaliana
Krishna, P., & Gloor, G. B. (2001) · Cell Stress and Chaperones · doi:10.1379/1466-1268(2001)006 · Cited by 360
Chaperones and aging: role in neurodegeneration and in other civilizational diseases
Sőti, C., & Csermely, P. (2002) · Neurochemistry International · doi:10.1016/s0197-0186(02)00043-8 · Cited by 109
REPLICATED EVOLUTION OF INTEGRATED PLASTIC RESPONSES DURING EARLY ADAPTIVE DIVERGENCE
Parsons, K. J., & Robinson, B. W. (2006) · Evolution · doi:10.1111/j.0014-3820.2006.tb01158.x · Cited by 109
Jablonski, D. (2005) · Journal of Experimental Zoology Part B: Molecular and Developmental Evolution · doi:10.1002/jez.b.21075 · Cited by 108
Quality control and fate determination of Hsp90 client proteins
Theodoraki, M. A., & Caplan, A. J. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.08.006 · Cited by 116
THE RELATIONSHIP BETWEEN FLUCTUATING ASYMMETRY AND ENVIRONMENTAL VARIANCE IN RHESUS MACAQUE SKULLS
Willmore, K. E., Klingenberg, C. P., & Hallgrímsson, B. (2005) · Evolution · doi:10.1111/j.0014-3820.2005.tb01763.x · Cited by 108
Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs
Leach, M. D., Klipp, E., Cowen, L. E., & Brown, A. J. P. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2875 · Cited by 107
The Relations between Genetics and Epigenetics
Morange, M. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb04911.x · Cited by 107
An erythroid chaperone that facilitates folding of α-globin subunits for hemoglobin synthesis
Yu, X., Kong, Y., Doré, L. C., Abdulmalik, O. Y., Katein, A. M., Zhou, S., Choi, J. K., Gell, D. A., Mackay, J. P., Gow, A. J., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31664 · Cited by 107
Leander, B. S., & Keeling, P. J. (2004) · Journal of Phycology · doi:10.1111/j.1529-8817.2004.03129.x · Cited by 107
Phenotypic plasticity can facilitate adaptive evolution in gene regulatory circuits
Espinosa‐Soto, C., Martin, O., & Wagner, A. (2011) · BMC Evolutionary Biology · doi:10.1186/1471-2148-11-5 · Cited by 109
Gassen, N. C., Fries, G. R., Zannas, A. S., Hartmann, J., Zschocke, J., Hafner, K., Carrillo‐Roa, T., Steinbacher, J., Preißinger, S. N., Hoeijmakers, L., et al. (2015) · Science Signaling · doi:10.1126/scisignal.aac7695 · Cited by 109
Protein aggregation as a paradigm of aging
Lindner, A. B., & Démarez, A. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.06.005 · Cited by 111
Disaggregating Chaperones: An Unfolding Story
Sharma, S., Christen, P., & Goloubinoff, P. (2009) · Current Protein and Peptide Science · doi:10.2174/138920309789351930 · Cited by 109
Dawson, M. N., & Martin, L. E. (2001) · Hydrobiologia · doi:10.1023/a:1011869215330 · Cited by 106
Selective apoptosis of tandemly duplicated FLT3-transformed leukemia cells by Hsp90 inhibitors
Minami, Y., Kiyoi, H., Yamamoto, Y., Yamamoto, K., Ueda, R., Saito, H., & Naoe, T. (2002) · Leukemia · doi:10.1038/sj.leu.2402558 · Cited by 106
Biological emergences: evolution by natural experiment
(2007) · Choice Reviews Online · doi:10.5860/choice.45-1451 · Cited by 106
Developmental nonlinearity drives phenotypic robustness
Green, R. M., Fish, J. L., Young, N. M., Smith, F. J., Roberts, B., Dolan, K., Choi, I., Leach, C. L., Gordon, P., Cheverud, J. M., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-02037-7 · Cited by 106
Molecular mechanisms of paralogous compensation and the robustness of cellular networks
Diss, G., Ascencio, D., DeLuna, A., & Landry, C. R. (2013) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22555 · Cited by 110
Vizeacoumar, F. J., van Dyk, N., Vizeacoumar, F. S., Cheung, V., Li, J., Sydorskyy, Y., Case, N., Li, Z., Datti, A., Nislow, C., et al. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.200909013 · Cited by 105
Condelli, V., Crispo, F., Pietrafesa, M., Lettini, G., Matassa, D. S., Esposito, F., Landriscina, M., & Maddalena, F. (2019) · Cells · doi:10.3390/cells8060532 · Cited by 107
Samakovli, D., Tichá, T., Vavrdová, T., Ovečka, M., Luptovčiak, I., Zapletalová, V., Kuchařová, A., Křenek, P., Krasylenko, Y. A., Margaritopoulou, T., et al. (2020) · Molecular Plant · doi:10.1016/j.molp.2020.01.001 · Cited by 107
HSP90 AND THE QUANTITATIVE VARIATION OF WING SHAPE IN DROSOPHILA MELANOGASTER
Debat, V., Milton, C. C., Rutherford, S., Klingenberg, C. P., & Hoffmann, A. A. (2006) · Evolution · doi:10.1554/06-045.1 · Cited by 108
Self-citationGarcia, S. M. D. A., Casanueva, O., Silva, M. C., Amaral, M. D., & Morimoto, R. I. (2007) · Genes & Development · doi:10.1101/gad.1575307 · Cited by 106
The role of genes domesticated from LTR retrotransposons and retroviruses in mammals
Kaneko-Ishino, T., & Ishino, F. (2012) · Frontiers in Microbiology · doi:10.3389/fmicb.2012.00262 · Cited by 104
Lachowiec, J., Queitsch, C., & Kliebenstein, D. J. (2015) · Annals of Botany · doi:10.1093/aob/mcv151 · Cited by 106
It’s not magic – Hsp90 and its effects on genetic and epigenetic variation
Zabinsky, R. A., Mason, G. A., Queitsch, C., & Jarosz, D. F. (2018) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2018.05.015 · Cited by 106
Hallgrímsson, B., Brown, J. J. Y., Ford-Hutchinson, A. F., Sheets, H. D., Zelditch, M. L., & Jirik, F. R. (2006) · Evolution & Development · doi:10.1111/j.1525-142x.2006.05075.x · Cited by 104
The evolutionary dynamics of evolvability in a gene network model
Draghi, J. A., & Wagner, G. P. (2008) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2008.01663.x · Cited by 104
Impact of gut microbiota on the fly’s germ line
Elgart, M., Stern, S., Salton, O., Gnainsky, Y., Heifetz, Y., & Soen, Y. (2016) · Nature Communications · doi:10.1038/ncomms11280 · Cited by 106
The developmental-genetics of canalization
Hallgrímsson, B., Green, R. M., Katz, D. C., Fish, J. L., Bernier, F. P., Roseman, C. C., Young, N. M., Cheverud, J. M., & Marcucio, R. (2018) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2018.05.019 · Cited by 106
Pauwels, K., Stoks, R., & Meester, L. D. (2005) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2005.00890.x · Cited by 103
Sørensen, J. G. (2010) · Current Zoology · doi:10.1093/czoolo/56.6.703 · Cited by 103
Phenotypic heterogeneity can enhance rare‐cell survival in ‘stress‐sensitive’ yeast populations
Bishop, A. L., Rab, F. A., Sumner, E. R., & Avery, S. V. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05504.x · Cited by 108
Chemical chaperones assist intracellular folding to buffer mutational variations
Bandyopadhyay, A., Saxena, K., Kasturia, N., Dalal, V., Bhatt, N. R., Rajkumar, A., Maity, S., Sengupta, S., & Chakraborty, K. (2012) · Nature Chemical Biology · doi:10.1038/nchembio.768 · Cited by 101
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Mossman, J. A., Biancani, L. M., Zhu, C.-T., & Rand, D. M. (2016) · Genetics · doi:10.1534/genetics.116.187286 · Cited by 101
Selection enhances protein evolvability by increasing mutational robustness and foldability
Zheng, J., Guo, N., & Wagner, A. (2020) · Science · doi:10.1126/science.abb5962 · Cited by 104
Heat-shock protein 90 inhibitors as novel cancer chemotherapeutic agents
Neckers, L., & Neckers, K. (2002) · Expert Opinion on Emerging Drugs · doi:10.1517/14728214.7.2.277 · Cited by 104
Deciphering morphology in Triatominae: The evolutionary signals
Dujardin, J., Costa, J. F., Bustamante, D., Jaramillo, N., & Catalá, S. (2008) · Acta Tropica · doi:10.1016/j.actatropica.2008.09.026 · Cited by 102
Ledón‐Rettig, C. C., Pfennig, D. W., & Crespi, E. J. (2010) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2010.0877 · Cited by 101
Apoptosis, necrosis and cellular senescence: chaperone occupancy as a potential switch
Sőti, C., Sreedhar, A. S., & Csermely, P. (2003) · Aging Cell · doi:10.1046/j.1474-9728.2003.00031.x · Cited by 101
Ragland, G. J., Almskaar, K., Vertacnik, K. L., Gough, H. M., Feder, J. L., Hahn, D. A., & Schwarz, D. (2015) · Molecular Ecology · doi:10.1111/mec.13191 · Cited by 101
Snails in the sun: Strategies of terrestrial gastropods to cope with hot and dry conditions
Schweizer, M., Triebskorn, R. A., & Köhler, H. (2019) · Ecology and Evolution · doi:10.1002/ece3.5607 · Cited by 100
Tonsor, S. J., Elnaccash, T. W., & Scheiner, S. M. (2013) · Evolution · doi:10.1111/evo.12175 · Cited by 100
Advances in chromatin remodeling and human disease
Cho, K. S., Elizondo, L. I., & Boerkoel, C. F. (2004) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2004.04.015 · Cited by 102
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Variation of tooth number in mammalian dentition: connecting genetics, development, and evolution
Line, S. R. P. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03036.x · Cited by 99
Shi, W. L., Feng, L., Dong, S., Ning, Z., Hua, Y., Liu, L., Chen, Z., & Meng, Z. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-00604-y · Cited by 101
Molecular Aspects of the Stress Response: Chaperones, Membranes and Networks
Csermely, P., & VÃgh, L. (2007) · Springer eBooks · doi:10.1007/978-0-387-39975-1 · Cited by 100
Domart-Coulon, I. J., Traylor‐Knowles, N., Peters, E. C., Elbert, D. C., Downs, C. A., Price, K. L., Stubbs, J. E., McLaughlin, S., Cox, E. F., Aeby, G. S., et al. (2006) · Coral Reefs · doi:10.1007/s00338-006-0133-6 · Cited by 99
Suzuki, I., Kanesaki, Y., Hayashi, H., Hall, J. J., Simon, W. J., Slabas, A. R., & Murata, N. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.104.059097 · Cited by 99
Phenotypic plasticity in the range-margin population of the lycaenid butterfly Zizeeria maha
Otaki, J. M., Hiyama, A., Iwata, M., & Kudo, T. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-252 · Cited by 98
Dworkin, I. M., Pálsson, A., Birdsall, K., & Gibson, G. C. (2003) · Current Biology · doi:10.1016/j.cub.2003.10.001 · Cited by 99
Cao, D., Froehlich, J. E., Zhang, H., & Cheng, C. (2003) · The Plant Journal · doi:10.1046/j.1365-313x.2003.016011.x · Cited by 98
Hsp90 Phosphorylation Is Linked to Its Chaperoning Function
Zhao, Y.-G., Gilmore, R., Leone, G. W., Coffey, M. C., Weber, B., & Lee, P. W. K. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m105562200 · Cited by 98
Heat shock proteins and aging in Drosophila melanogaster
Morrow, G., & Tanguay, R. M. (2003) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2003.09.023 · Cited by 101
Clark, M. S., & Peck, L. S. (2009) · Cell Stress and Chaperones · doi:10.1007/s12192-009-0117-x · Cited by 100
Hsp90 Inhibitors in the Clinic
Pacey, S., Banerj, U., Judson, I. R., & Workman, P. (2005) · Springer eBooks · doi:10.1007/3-540-29717-0_14 · Cited by 98
Nathan, D. F., Vos, M. H., & Lindquist, S. L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.4.1409 · Cited by 96
Self-citationChen, J., Nolte, V., & Schlötterer, C. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1004883 · Cited by 97
Mechanisms of mutational robustness in transcriptional regulation
Payne, J. L., & Wagner, A. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00322 · Cited by 97
Selection Transforms the Landscape of Genetic Variation Interacting with Hsp90
Geiler‐Samerotte, K., Zhu, Y. O., Goulet‐Scott, B. E., Hall, D. W., & Siegal, M. L. (2016) · PLoS Biology · doi:10.1371/journal.pbio.2000465 · Cited by 96
Cloutier, P., & Coulombe, B. (2013) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2013.02.010 · Cited by 96
Hsp90 phosphorylation, Wee1 and the cell cycle
Mollapour, M., Tsutsumi, S., & Neckers, L. (2010) · Cell Cycle · doi:10.4161/cc.9.12.12054 · Cited by 96
Huang, L., Min, J., Masters, S. C., Mivechi, N. F., & Moskophidis, D. (2007) · genesis · doi:10.1002/dvg.20319 · Cited by 97
Koga, F., Kihara, K., & Neckers, L. (2009) · PubMed · Cited by 94
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Klimczak, M., Biecek, P., Żylicz, M., & Żylicz, M. (2019) · Scientific Reports · doi:10.1038/s41598-019-43556-1 · Cited by 93
Ludwig‐Müller, J., Krishna, P., & Forreiter, C. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.123.3.949 · Cited by 93
Small heat shock protein expression and functions during development
Morrow, G., & Tanguay, R. M. (2012) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2012.03.009 · Cited by 93
The fungal Achilles’ heel: targeting Hsp90 to cripple fungal pathogens
Cowen, L. E. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.03.005 · Cited by 102
Genes Confer Similar Robustness to Environmental, Stochastic, and Genetic Perturbations in Yeast
Lehner, B. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009035 · Cited by 94
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Stechmann, A., & Cavalier‐Smith, T. (2003) · Journal of Molecular Evolution · doi:10.1007/s00239-003-2490-x · Cited by 94
Parkinson, S. E., Gross, S., & Hollick, J. B. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.06.004 · Cited by 93
Cell cycle transition under stress conditions controlled by vertebrate heat shock factors
Nakai, A., & Ishikawa, T. (2001) · The EMBO Journal · doi:10.1093/emboj/20.11.2885 · Cited by 92
Molecular chaperones as regulatory elements of cellular networks
Sőti, C., Pál, C., Papp, B., & Csermely, P. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.02.012 · Cited by 93
Diachronic Biology Meets Evo-Devo: C. H. Waddington's Approach to Evolutionary Developmental Biology
Gilbert, S. F. (2000) · American Zoologist · doi:10.1093/icb/40.5.729 · Cited by 92
Genetics of microenvironmental canalization in Arabidopsis thaliana
Hall, M. C., Dworkin, I. M., Ungerer, M. C., & Purugganan, M. D. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701936104 · Cited by 92
Hsp90 as a Target for Drug Development
Chaudhury, S., Welch, T. R., & Blagg, B. S. J. (2006) · ChemMedChem · doi:10.1002/cmdc.200600112 · Cited by 93
Developmental capacitance, genetic accommodation, and adaptive evolution
Moczek, A. P. (2007) · Evolution & Development · doi:10.1111/j.1525-142x.2007.00162.x · Cited by 92
Comprehensive fitness maps of Hsp90 show widespread environmental dependence
Flynn, J. M., Rossouw, A., Cote-Hammarlof, P., Fragata, I., Mavor, D., Hollins, C., Bank, C., & Bolon, D. N. (2020) · eLife · doi:10.7554/elife.53810 · Cited by 91
Shahinas, D., Liang, M., Datti, A., & Pillai, D. R. (2010) · Journal of Medicinal Chemistry · doi:10.1021/jm901796s · Cited by 91
HSP90: Enabler of Cancer Adaptation
Jaeger, A. M., & Whitesell, L. J. (2018) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-030518-055533 · Cited by 92
The Hsp70-Chaperone Machines in Bacteria
Mayer, M. P. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.694012 · Cited by 91
PHOX2B Germline and Somatic Mutations in Late-Onset Central Hypoventilation Syndrome
Trochet, D., de Pontual, L., Straus, C., Gozal, D., Trang, H., Landrieu, P., Münnich, A., Lyonnet, S., Gaultier, C., & Amiel, J. (2007) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200707-1079oc · Cited by 91
Metadata
- Authors
- Rutherford, S. L., & Lindquist, S.
- Affiliations
- Howard Hughes Medical Institute (US)
- Venue
- Nature
- Published
- 1998-11
- Volume
- 396
- Issue
- 6709
- Pages
- 336-342
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1554180547
- Cited by
- 2,270
- References
- 38
- Citations by year
- 2026: 45 · 2025: 57 · 2024: 53 · 2023: 58 · 2022: 60 · 2021: 54 · 2020: 56 · 2019: 86 · 2018: 95 · 2017: 77 · 2016: 84 · 2015: 93 · 2014: 104 · 2013: 108 · 2012: 93
- FWCI
- 18.89
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Morphological variations and asymmetry
- Keywords
- HSP90, morphological evolution, cryptic genetic variation, Drosophila, developmental pathways, signal transduction, genetic background effects, temperature effects, morphological variation
- MeSH terms
- Animals, Drosophila, Heat-Shock Proteins, Models, Genetic, Mutation, Phenotype, Temperature, Genetic Variation, HSP90 Heat-Shock Proteins, Directed Molecular Evolution, 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.
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