Under cover: causes, effects and implications of Hsp90‐mediated genetic capacitance

Sangster, Todd A.; Lindquist, Susan; Queitsch, Christine

doi:10.1002/bies.20020

Cited by 252Heat shock proteins researchEvolution and Genetic DynamicsRNA and protein synthesis mechanisms

Under cover: causes, effects and implications of Hsp90‐mediated genetic capacitance

Sangster, Todd A., Lindquist, Susan, Queitsch, Christine·2004·BioEssays

DOI 10.1002/bies.20020

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Abstract

The environmentally responsive molecular chaperone Hsp90 assists the maturation of many key regulatory proteins. An unexpected consequence of this essential biochemical function is that genetic variation can accumulate in genomes and can remain phenotypically silent until Hsp90 function is challenged. Notably, this variation can be revealed by modest environmental change, establishing an environmentally responsive exposure mechanism. The existence of diverse cryptic polymorphisms with a plausible exposure mechanism in evolutionarily distant lineages has implications for the pace and nature of evolutionary change. Chaperone‐mediated storage and release of genetic variation is undoubtedly rooted in protein‐folding phenomena. As we discuss, proper protein folding crucially affects the trajectory from genotype to phenotype. Indeed, the impact of protein quality‐control mechanisms and other fundamental cellular processes on evolution has heretofore been overlooked. A true understanding of evolutionary processes will require an integration of current evolutionary paradigms with the many new insights accruing in protein science. BioEssays 26:348–362, 2004. © 2004 Wiley Periodicals, Inc.

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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.
“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 [131]
Hsp90's role as a capacitor for variation has been observed in diverse eukaryotes including flies, plants, and fungi.
“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 [131]
The ability of an organism to tolerate environmental and genetic variation may be dependent on phenotypic capacitors, a class of genes whose inactivation may increase phenotypic variation among genetically diverse individuals in a population.
“The ability of an organism to tolerate environmental and genetic variation may be dependent on phenotypic capacitors, a class of genes whose inactivation may increase phenotypic variation among genetically diverse individuals in a population (18).”
From A global genetic interaction network maps a wiring diagram of cellular function (2016) · cites this paper as [18]
Hsp90, the canonical capacitor, is a molecular chaperone controlling numerous signaling pathways and thus is considered a multi-functional or pleiotropic gene.
“Hsp90, the canonical capacitor, is a molecular chaperone controlling numerous signaling pathways and thus is considered a multi-functional or pleiotropic gene (18).”
From A global genetic interaction network maps a wiring diagram of cellular function (2016) · cites this paper as [18]

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Hsp90 and Chromatin: Where is the Link?
Sangster, T. A., Queitsch, C., & Lindquist, S. L. (2003) · Cell Cycle · doi:10.4161/cc.2.3.400 · Cited by 29 · see citing works
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Gene Conversion may aid Adaptive Peak Shifts
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GENETIC DISSECTION OF THE Hsp70 CHAPERONE SYSTEM OF YEAST
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HSP90 and the chaperoning of cancer
Whitesell, L., & Lindquist, S. L. (2005) · Nature Reviews Cancer · doi:10.1038/nrc1716 · Cited by 2,502 · see citing works
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Transgenerational Epigenetic Inheritance: Prevalence, Mechanisms, and Implications for the Study of Heredity and Evolution
Jablonka, E., & Raz, G. (2009) · The Quarterly Review of Biology · doi:10.1086/598822 · Cited by 1,659 · see citing works
A global genetic interaction network maps a wiring diagram of cellular function
Costanzo, M., VanderSluis, B., Koch, E. N., Baryshnikova, A., Pons, C., Tan, G., Wang, W., Usaj, M., Hanchard, J., Lee, S. D., et al. (2016) · Science · doi:10.1126/science.aaf1420 · Cited by 1,240 · see citing works
Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation
López-Maury, L., Marguerat, S., & Bähler, J. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2398 · Cited by 1,061 · see citing works
Pathways of chaperone-mediated protein folding in the cytosol
Young, J. C., Agashe, V. R., Siegers, K., & Hartl, F. U. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1492 · Cited by 1,101 · see citing works
Phenotypic plasticity's impacts on diversification and speciation
Pfennig, D. W., Wund, M. A., Snell-Rood, E. C., Cruickshank, T., Schlichting, C. D., & Moczek, A. P. (2010) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2010.05.006 · Cited by 1,170 · see citing works
Hsp90 Potentiates the Rapid Evolution of New Traits: Drug Resistance in Diverse Fungi
Cowen, L. E., & Lindquist, S. (2005) · Science · doi:10.1126/science.1118370 · Cited by 698 · see citing works
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Missense meanderings in sequence space: a biophysical view of protein evolution
DePristo, M. A., Weinreich, D. M., & Hartl, D. L. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1672 · Cited by 651 · see citing works
A REASSESSMENT OF GENETIC LIMITS TO EVOLUTIONARY CHANGE
Blows, M. W., & Hoffmann, A. A. (2005) · Ecology · doi:10.1890/04-1209 · Cited by 607 · see citing works
Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future
Dongen, S. V. (2006) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2006.01175.x · Cited by 560 · see citing works
Prions as adaptive conduits of memory and inheritance
Shorter, J., & Lindquist, S. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1616 · Cited by 555 · see citing works
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The Hsp90 chaperone machinery: Conformational dynamics and regulation by co-chaperones
Li, J., Soroka, J., & Buchner, J. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.09.003 · Cited by 498 · see citing works
Diverse Cellular Functions of the Hsp90 Molecular Chaperone Uncovered Using Systems Approaches
McClellan, A. J., Xia, Y., Deutschbauer, A. M., Davis, R. W., Gerstein, M., & Frydman, J. (2007) · Cell · doi:10.1016/j.cell.2007.07.036 · Cited by 474 · see citing works
Embryo stability and vulnerability in an always changing world
Hamdoun, A. M., & Epel, D. D. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610108104 · Cited by 390 · see citing works
Chaperonin overexpression promotes genetic variation and enzyme evolution
Tokuriki, N., & Tawfik, D. S. (2009) · Nature · doi:10.1038/nature08009 · Cited by 347 · see citing works
Robustness: mechanisms and consequences
Masel, J., & Siegal, M. L. (2009) · Trends in Genetics · doi:10.1016/j.tig.2009.07.005 · Cited by 348 · see citing works
Hsp90 and Environmental Stress Transform the Adaptive Value of Natural Genetic Variation
Jarosz, D. F., & Lindquist, S. (2010) · Science · doi:10.1126/science.1195487 · Cited by 346 · see citing works
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Hsp90: Structure and Function
Jackson, S. (2012) · Topics in current chemistry · doi:10.1007/128_2012_356 · Cited by 334 · see citing works
The Genetics and Evolution of Fluctuating Asymmetry
Leamy, L. J., & Klingenberg, C. P. (2005) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.36.102003.152640 · Cited by 327 · see citing works
The evolution of fungal drug resistance: modulating the trajectory from genotype to phenotype.
Cowen, L. E. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1835 · Cited by 311 · see citing works
Network Hubs Buffer Environmental Variation in Saccharomyces cerevisiae
Levy, S. F., & Siegal, M. L. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060264 · Cited by 279 · see citing works
Hsp70 chaperones accelerate protein translocation and the unfolding of stable protein aggregates by entropic pulling
Rios, P. D. L., Ben‐Zvi, A., Slutsky, O., Azem, A., & Goloubinoff, P. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510496103 · Cited by 268 · see citing works
Heat shock proteins and heat shock factor 1 in carcinogenesis and tumor development: an update
Ciocca, D. R., Arrigo, A. P., & Calderwood, S. K. (2012) · Archives of Toxicology · doi:10.1007/s00204-012-0918-z · Cited by 264 · see citing works
Hidden Reaction Norms, Cryptic Genetic Variation, and Evolvability
Schlichting, C. D. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1438.010 · Cited by 261 · see citing works
Hop: more than an Hsp70/Hsp90 adaptor protein
Odunuga, O. O., Longshaw, V. M., & Blatch, G. L. (2004) · BioEssays · doi:10.1002/bies.20107 · Cited by 224 · see citing works
Microevolution and Ecotoxicology of Metals in Invertebrates
Morgan, A. J., Kille, P., & Stürzenbaum, S. R. (2007) · Environmental Science & Technology · doi:10.1021/es061992x · Cited by 207 · see citing works
The HSP90 chaperone complex, an emerging force in plant development and phenotypic plasticity
Sangster, T. A., & Queitsch, C. (2004) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2004.11.012 · Cited by 205 · see citing works
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Proposal for a role of the Hsp90/Hsp70-based chaperone machinery in making triage decisions when proteins undergo oxidative and toxic damage
Pratt, W. B., Morishima, Y., Peng, H., & Osawa, Y. (2010) · Experimental Biology and Medicine · doi:10.1258/ebm.2009.009250 · Cited by 201 · see citing works
New insights into the mechanism of heat shock response activation
Shamovsky, I., & Nudler, E. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-7458-y · Cited by 197 · see citing works
Developmental plasticity mirrors differences among taxa in spadefoot toads linking plasticity and diversity
Gómez-Mestre, I., & Buchholz, D. R. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603562103 · Cited by 190 · see citing works
Oncogenic mutant forms of EGFR: Lessons in signal transduction and targets for cancer therapy
Pines, G., Köstler, W. J., & Yarden, Y. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.04.019 · Cited by 187 · see citing works
An Improved, Bias-Reduced Probabilistic Functional Gene Network of Baker's Yeast, Saccharomyces cerevisiae
Lee, I., Li, Z., & Marcotte, E. M. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000988 · Cited by 183 · see citing works
NLR sensors meet at the SGT1–HSP90 crossroad
Kadota, Y., Shirasu, K., & Guérois, R. (2010) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2009.12.005 · Cited by 181 · see citing works
Protein Homeostasis and the Phenotypic Manifestation of Genetic Diversity: Principles and Mechanisms
Jarosz, D. F., Taipale, M., & Lindquist, S. (2010) · Annual Review of Genetics · doi:10.1146/annurev.genet.40.110405.090412 · Cited by 179 · see citing works
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HSP90 affects the expression of genetic variation and developmental stability in quantitative traits
Sangster, T. A., Salathia, N., Undurraga, S., Milo, R., Schellenberg, K., Lindquist, S., & Queitsch, C. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712200105 · Cited by 174 · see citing works
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Recent insights into R gene evolution
McDowell, J. M., & Simon, S. A. (2006) · Molecular Plant Pathology · doi:10.1111/j.1364-3703.2006.00342.x · Cited by 175 · see citing works
Explaining bathymetric diversity patterns in marine benthic invertebrates and demersal fishes: physiological contributions to adaptation of life at depth
Brown, A., & Thatje, S. (2013) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12061 · Cited by 170 · see citing works
Précis ofEvolution in Four Dimensions
Jablonka, E., & Lamb, M. J. (2007) · Behavioral and Brain Sciences · doi:10.1017/s0140525x07002221 · Cited by 166 · see citing works
Genetic Architecture of Hsp90-Dependent Drug Resistance
Cowen, L. E., Carpenter, A. E., Matangkasombut, O., Fink, G. R., & Lindquist, S. (2006) · Eukaryotic Cell · doi:10.1128/ec.00274-06 · Cited by 159 · see citing works
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Phenotypic Diversity and Altered Environmental Plasticity in Arabidopsis thaliana with Reduced Hsp90 Levels
Sangster, T. A., Bahrami, A. K., Wilczek, A. M., Watanabe, E., Schellenberg, K., McLellan, C. A., Kelley, A. M., Kong, S. W., Queitsch, C., & Lindquist, S. L. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000648 · Cited by 158 · see citing works
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Hsp90 Selectively Modulates Phenotype in Vertebrate Development
Yeyati, P. L., Bancewicz, R. M., Maule, J., & van Heyningen, V. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0030043 · Cited by 159 · see citing works
Hsp70 Structure, Function, Regulation and Influence on Yeast Prions
Sharma, D., & Masison, D. C. (2009) · Protein and Peptide Letters · doi:10.2174/092986609788490230 · Cited by 156 · see citing works
Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variation
Gangaraju, V. K., Yin, H., Weiner, M. M., Wang, J., Huang, X., & Lin, H. (2010) · Nature Genetics · doi:10.1038/ng.743 · Cited by 156 · see citing works
Mutation dynamics and fitness effects followed in single cells
Robert, L., Ollion, J., Robert, J., Song, X., Matić, I., & Elez, M. (2018) · Science · doi:10.1126/science.aan0797 · Cited by 147 · see citing works
Genomics of Developmental Plasticity in Animals
Lafuente, E., & Beldade, P. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00720 · Cited by 147 · see citing works
A Rhizosphere Fungus Enhances Arabidopsis Thermotolerance through Production of an HSP90 Inhibitor
McLellan, C. A., Turbyville, T. J., Wijeratne, E. M. K., Kerschen, A., Vierling, E., Queitsch, C., Whitesell, L. J., & Gunatilaka, A. A. L. (2007) · PLANT PHYSIOLOGY · doi:10.1104/pp.107.101808 · Cited by 144 · see citing works
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Transient Exposure to Low Levels of Insecticide Affects Metabolic Networks of Honeybee Larvae
Derecka, K., Blythe, M., Malla, S., Genereux, D. P., Guffanti, A., Pavan, P., Moles, A., Snart, C. J. P., Ryder, T., Ortori, C. A., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068191 · Cited by 148 · see citing works
Thermal Control of Microbial Development and Virulence: Molecular Mechanisms of Microbial Temperature Sensing
Shapiro, R. S., & Cowen, L. E. (2012) · mBio · doi:10.1128/mbio.00238-12 · Cited by 145 · see citing works
Evolvable signaling networks of receptor tyrosine kinases: relevance of robustness to malignancy and to cancer therapy
Amit, I., Wides, R., & Yarden, Y. (2007) · Molecular Systems Biology · doi:10.1038/msb4100195 · Cited by 144 · see citing works
HSP90-buffered genetic variation is common in Arabidopsis thaliana
Sangster, T. A., Salathia, N., Lee, H. N., Watanabe, E., Schellenberg, K., Morneau, K., Wang, H., Undurraga, S., Queitsch, C., & Lindquist, S. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712210105 · Cited by 131 · see citing works
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Genetic predisposition to cancer — insights from population genetics
Frank, S. A. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1450 · Cited by 132 · see citing works
Sgt1p Is a Unique Co-chaperone That Acts as a Client Adaptor to Link Hsp90 to Skp1p
Catlett, M. G., & Kaplan, K. B. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m603847200 · Cited by 126 · see citing works
Overexpression of AtHsp90.2, AtHsp90.5 and AtHsp90.7 in Arabidopsis thaliana enhances plant sensitivity to salt and drought stresses
Song, H., Zhao, R., Fan, P., Wang, X., Chen, X., & Li, Y. (2009) · Planta · doi:10.1007/s00425-008-0886-y · Cited by 120 · see citing works
The integration of activity in saline environments: problems and perspectives
Cheeseman, J. M. (2013) · Functional Plant Biology · doi:10.1071/fp12285 · Cited by 120 · see citing works
Intracellular protozoan parasites of humans: the role of molecular chaperones in development and pathogenesis.
Shonhai, A., Maier, A., Przyborski, J., & Blatch, G. (2011) · Protein Peptide Letters · doi:10.2174/092986611794475002 · Cited by 109 · see citing works
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 · see citing works
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Hsp90: A New Player in DNA Repair?
Pennisi, R., Ascenzi, P., & Di Masi, A. (2015) · Biomolecules · doi:10.3390/biom5042589 · Cited by 112 · see citing works
Evolutionary innovations in the fossil record: the intersection of ecology, development, and macroevolution
Jablonski, D. (2005) · Journal of Experimental Zoology Part B: Molecular and Developmental Evolution · doi:10.1002/jez.b.21075 · Cited by 108 · see citing works
Keeping up NF-κB appearances: Epigenetic control of immunity or inflammation-triggered epigenetics
Berghe, W. V., Ndlovu, ’. N., Hoya-Arias, R., Dijsselbloem, N., Gerlo, S., & Haegeman, G. (2006) · Biochemical Pharmacology · doi:10.1016/j.bcp.2006.07.012 · Cited by 108 · see citing works
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 · see citing works
Plant Responses to High Temperature
Larkindale, J., Mishkind, M., & Vierling, E. (2005) · doi:10.1002/9780470988503.ch5 · Cited by 105 · see citing works
Neuronal signaling modulates protein homeostasis in Caenorhabditis elegans post-synaptic muscle cellsPreprint
Garcia, 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 105 · see citing works
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 104 · see citing works
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Intercellular competition and the inevitability of multicellular aging
Nelson, P., & Masel, J. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1618854114 · Cited by 100 · see citing works
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 99 · see citing works
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 93 · see citing works
Inhibition of Hsp90: A Multitarget Approach to Radiosensitization
Camphausen, K. A., & Tofilon, P. J. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-0632 · Cited by 94 · see citing works
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 92 · see citing works
Is it good noise? The role of developmental instability in the shaping of a root system
Forde, B. (2009) · Journal of Experimental Botany · doi:10.1093/jxb/erp265 · Cited by 91 · see citing works
Insights into function and regulation of small heat shock protein 25 (HSPB1) in a mouse model with targeted gene disruption
Huang, L., Min, J., Masters, S. C., Mivechi, N. F., & Moskophidis, D. (2007) · genesis · doi:10.1002/dvg.20319 · Cited by 94 · see citing works
The unforeseen challenge: from genotype-to-phenotype in cell populations
Braun, E. (2015) · Reports on Progress in Physics · doi:10.1088/0034-4885/78/3/036602 · Cited by 88 · see citing works
Modelling the Role of the Hsp70/Hsp90 System in the Maintenance of Protein Homeostasis
Proctor, C. J., & Lorimer, I. A. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022038 · Cited by 87 · see citing works
On the Nature and Evolutionary Impact of Phenotypic Robustness Mechanisms
Siegal, M. L., & Leu, J. (2014) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-120213-091705 · Cited by 85 · see citing works
Hsp70 molecular chaperones are required to support p53 tumor suppressor activity under stress conditions
Walerych, D., Olszewski, M. B., Gutkowska, M., Helwak, A., Żylicz, M., & Żylicz, M. (2009) · Oncogene · doi:10.1038/onc.2009.281 · Cited by 82 · see citing works
Antifungal activity of redox-active benzaldehydes that target cellular antioxidation
Jong Heon, K. I. M., Chan, K. L., Mahoney, N. E., & Campbell, B. C. (2011) · Annals of Clinical Microbiology and Antimicrobials · doi:10.1186/1476-0711-10-23 · Cited by 83 · see citing works
Unwinding by Local Strand Separation Is Critical for the Function of DEAD-Box Proteins as RNA Chaperones
Campo, M. D., Mohr, S., Jiang, Y., Jia, H., Jankowsky, E., & Lambowitz, A. M. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.04.043 · Cited by 82 · see citing works
Obesity and ADHD may represent different manifestations of a common environmental oversampling syndrome: a model for revealing mechanistic overlap among cognitive, metabolic, and inflammatory disorders
Bazar, K. A., Yun, A. J., Lee, P. Y., Daniel, S. M., & Doux, J. D. (2005) · Medical Hypotheses · doi:10.1016/j.mehy.2005.02.042 · Cited by 76 · see citing works
Metabolomic Signatures of Inbreeding at Benign and Stressful Temperatures inDrosophila melanogaster
Pedersen, K. S., Kristensen, T. N., Loeschcke, V., Petersen, B. O., Duus, J. Ø., Nielsen, N. C., & Malmendal, A. (2008) · Genetics · doi:10.1534/genetics.108.089144 · Cited by 76 · see citing works
Hsp90 is important for fecundity, longevity, and buffering of cryptic deleterious variation in wild fly populations
Chen, B., & Wagner, A. (2012) · BMC Evolutionary Biology · doi:10.1186/1471-2148-12-25 · Cited by 76 · see citing works
The evolutionary capacitor HSP90 buffers the regulatory effects of mammalian endogenous retroviruses
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Hsp90—From signal transduction to cell transformation
Brown, M. A., Zhu, L., Schmidt, C., & Tucker, P. W. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.08.054 · Cited by 73 · see citing works
Chemical Tools to Investigate Mechanisms Associated with HSP90 and HSP70 in Disease
Shrestha, L., Patel, H. J., & Chiosis, G. (2016) · Cell chemical biology · doi:10.1016/j.chembiol.2015.12.006 · Cited by 71 · see citing works
Protein evolution speed depends on its stability and abundance and on chaperone concentrations
Agozzino, L., & Dill, K. A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1810194115 · Cited by 64 · see citing works
Environmental factors affecting reproduction and development in ascidians and other protochordates
Bates, W. R. (2005) · Canadian Journal of Zoology · doi:10.1139/z04-164 · Cited by 63 · see citing works
HIGH TEMPERATURES REVEAL CRYPTIC GENETIC VARIATION IN A POLYMORPHIC FEMALE SPERM STORAGE ORGAN
Berger, D., Bauerfeind, S. S., Blanckenhorn, W. U., & Schäfer, M. A. (2011) · Evolution · doi:10.1111/j.1558-5646.2011.01392.x · Cited by 60 · see citing works
Lessons from Model Organisms: Phenotypic Robustness and Missing Heritability in Complex Disease
Queitsch, C., Carlson, K. D., & Girirajan, S. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003041 · Cited by 61 · see citing works
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Molecular mechanisms of robustness in plants
Lempe, J., Lachowiec, J., Sullivan, A. M., & Queitsch, C. (2012) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2012.12.002 · Cited by 61 · see citing works
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The origins of mutational robustness
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Authors: Sangster, T. A., Lindquist, S., & Queitsch, C.
Affiliations: University of Chicago (US)
Whitehead Institute for Biomedical Research (US)
Harvard University (US)
Corresponding author: Queitsch, Christine
ORCID: Queitsch, Christine
Venue: BioEssays
Publisher: Wiley
Published: 2004-03-26
Volume: 26
Issue: 4
Pages: 348-362
ISSN: 0265-9247 (ISSN-L)
1521-1878
DOI: 10.1002/bies.20020
OpenAlex: W2147056656
Cited by: 251
References: 112
Citations by year: 2026: 3 · 2025: 7 · 2024: 6 · 2023: 4 · 2022: 2 · 2021: 2 · 2020: 2 · 2019: 7 · 2018: 12 · 2017: 7 · 2016: 9 · 2015: 9 · 2014: 10 · 2013: 10 · 2012: 15
FWCI: 2.13
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: BioEssays (publishedVersion)
PubMed (publishedVersion)
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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
Keywords: HSP90, molecular chaperones, protein folding, protein quality control, phenotypic plasticity, environmental change, evolutionary change, genotype-phenotype correlation
MeSH terms: Animals, Drosophila melanogaster, Environment, Genotype, Humans, Models, Biological, Models, Genetic, Neoplasms, Phenotype, Polymorphism, Genetic, Temperature, Genetic Variation, Arabidopsis, Molecular Chaperones, HSP90 Heat-Shock Proteins

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