The Hsp90 Capacitor, Developmental Remodeling, and Evolution: The Robustness of Gene Networks and the Curious Evolvability of Metamorphosis

REFERENCES

• Agrawal A. F., Hadany L., Otto S. P. The evolution of plastic recombination. Genetics 2005; 171: 803–812
   PubMedGoogle Scholar
• Ali A., Bharadwaj S., O'Carroll R., Ovsenek N. HSP90 interacts with and regulates the activity of heat shock factor 1 in Xenopus oocytes. Mol Cell Biol 1998; 18: 4949–4960
   PubMed Web of Science ®Google Scholar
• Allen J., McAlister J. Testing rates of planktonic versus benthic predation in the field. J Exp Marine Biol Ecol 2007, (epub)
   Google Scholar
• Alon U., Surette M. G., Barkai N., Leibler S. Robustness in bacterial chemotaxis. Nature 1999; 397: 168–171
   PubMed Web of Science ®Google Scholar
• Arbeitman M. N., Hogness D. S. Molecular chaperones activate the Drosophila ecdysone receptor, an RXR heterodimer. Cell 2000; 101: 67–77
   PubMed Web of Science ®Google Scholar
• Baker M. E. Evolution of metamorphosis: role of environment on expression of mutant nuclear receptors and other signal-transduction proteins. Integr Comp Biol 2006; 46: 808–814
   PubMedGoogle Scholar
• Barkai N., Leibler S. Robustness in simple biochemical networks. Nature 1997; 387: 913–917
   PubMed Web of Science ®Google Scholar
• Barolo S., Posakony J. W. Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling. Genes Dev 2002; 16: 1167–1181
   PubMedGoogle Scholar
• Bergman A., Siegal M. L. Evolutionary capacitance as a general feature of complex gene networks. Nature 2003; 424: 549–552
   PubMed Web of Science ®Google Scholar
• Birnby D. A., Link E. M., Vowels J. J., Tian H., Colacurcio P. L., Thomas J. H. A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans. Genetics 2000; 155: 85–104
   PubMedGoogle Scholar
• Bishop C. D., Brandhorst B. P. NO/cGMP signaling and HSP90 activity represses metamorphosis in the sea urchin Lytechinus pictus. Biol Bull 2001; 201: 394–404
   PubMed Web of Science ®Google Scholar
• Bishop C. D., Brandhorst B. P. On nitric oxide signaling, metamorphosis, and the evolution of biphasic life cycles. Evol Dev 2003; 5: 542–550
   PubMed Web of Science ®Google Scholar
• Bishop C. D., Bates W. R., Brandhorst B. P. Regulation of metamorphosis in ascidians involves NO/cGMP signaling and HSP90. J Exp Zool 2001; 289: 374–384
   PubMedGoogle Scholar
• Bishop C. D., Huggett M. J., Heyland A., Hodin J., Brandhorst B. P. Interspecific variation in metamorphic competence in marine invertebrates: the significance for comparative investigations into the timing of metamorphosis. Integr Comp Biol 2006; 46: 662–682
   PubMed Web of Science ®Google Scholar
• Brunt S. A., Riehl R., Silver J. C. Steroid hormone regulation of the Achlya ambisexualis 85-kilodalton heat shock protein, a component of the Achlya steroid receptor complex. Mol Cell Biol 1990; 10: 273–281
   PubMedGoogle Scholar
• Brunt S. A., Perdew G. H., Toft D. O., Silver J. C. Hsp90-containing multiprotein complexes in the eukaryotic microbe Achlya. Cell Stress Chaperones 1998; 3: 44–56
   PubMedGoogle Scholar
• Carey C. C., Gorman K. F., Rutherford S. Modularity and intrinsic evolvability of Hsp90-buffered change. PLoS ONE 2006; 1: e76
   Google Scholar
• Cheung J., Smith D. F. Molecular chaperone interactions with steroid receptors: an update. Mol Endocrinol 2000; 14: 939–946
   PubMed Web of Science ®Google Scholar
• Chino Y., Saito M., Yamasu K., Suyemitsu T., Ishihara K. Formation of the adult rudiment of sea urchins is influenced by thyroid hormones. Dev Biol 1994; 161: 1–11
   PubMed Web of Science ®Google Scholar
• Csermely P., Schnaider T., Soti C., Prohaszka Z., Nardai G. The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther 1998; 79: 129–168
   PubMed Web of Science ®Google Scholar
• Cutforth T., Rubin G. M. Mutations in Hsp83 cdc37 impair signaling by the sevenless receptor tyrosine kinase in Drosophila. Cell 1994; 77: 1027–1036
   PubMed Web of Science ®Google Scholar
• Davidson B., Jacobs M., Swalla B. J. The individual as a module: Solitary to colonial transitions in metazoan evolution and development. Modularity in development and evolution, G. Schlosser, G. P. Wagner. University of Chicago Press, Chicago 2004; 443–465
   Google Scholar
• de Visser J. A., Hermisson J., Wagner G. P., Ancel Meyers L., Bagheri-Chaichian H., Blanchard J. L., Chao L., Cheverud J. M., Elena S. F., Fontana W., et al. Perspective: Evolution and detection of genetic robustness. Evolution Int J Org Evolution 2003; 57: 1959–972
   PubMed Web of Science ®Google Scholar
• Degnan S. M., Degnan B. M. The origin of the pelagobenthic metazoan life cycle: what's sex got to do with it?. Integr Comp Biol 2006; 46: 683–690
   PubMedGoogle Scholar
• Dickinson W. J., Seger J. Cause and effect in evolution. Nature 1999; 399: 30
   Google Scholar
• Dickson B., van der Straten A., Dominguez M., Hafen E. Mutations modulating raf signaling in Drosophila eye development. Genetics 1996; 142: 163–171
   PubMed Web of Science ®Google Scholar
• Duina A. A., Kalton H. M., Gaber R. F. Requirement for Hsp90 and a CyP-40-type cyclophilin in negative regulation of the heat shock response. J Biol Chem 1998; 273: 18974–18978
   PubMedGoogle Scholar
• Escriva H., Bertrand S., Laudet V. The evolution of the nuclear receptor superfamily. Essays Biochem 2004; 40: 11–26
   PubMed Web of Science ®Google Scholar
• Falconer D. S., Mackay T. F.C. Introduction to quantitative genetics. Longman, EssexEngland 1996
   Google Scholar
• Fares M. A., Ruiz-Gonzalez M. X., Moya A., Elena S. F., Barrio E. Endosymbiotic bacteria: groEL buffers against deleterious mutations. Nature 2002; 417: 398
   PubMed Web of Science ®Google Scholar
• Feder M. E., Krebs R. A. Ecological and evolutionary physiology of heat shock proteins and the stress response in Drosophila: complementary insights from genetic engineering and natural variation. Exs 1997; 83: 155–173
   PubMedGoogle Scholar
• Ferrell J. E., Jr. Tripping the switch fantastic: how a protein kinase cascade can convert graded inputs into switch-like outputs. Trends Biochem Sci 1996; 21: 460–466
   PubMed Web of Science ®Google Scholar
• Ferrell J. E., Jr. How regulated protein translocation can produce switch-like responses. Trends Biochem Sci 1998; 23: 461–465
   PubMedGoogle Scholar
• Frankel J., Nelsen E. M. The effects of supraoptimal temperatures on population growth and cortical patterning in Tetrahymena pyriformis Tetrahymena thermophila: a comparison. J Eukaryot Microbiol 2001; 48: 135–146
   PubMedGoogle Scholar
• Frankel J., Williams N. E., Nelsen E. M., Keeling P. J. An evaluation of Hsp90 as a mediator of cortical patterning in Tetrahymena. J Eukaryot Microbiol 2001; 48: 147–160
   PubMedGoogle Scholar
• Freeman B. C., Yamamoto K. R. Continuous recycling: a mechanism for modulatory signal transduction. Trends Biochem Sci 2001; 26: 285–290
   PubMed Web of Science ®Google Scholar
• Freeman B. C., Yamamoto K. R. Disassembly of transcriptional regulatory complexes by molecular chaperones. Science 2002; 296: 2232–2235
   PubMed Web of Science ®Google Scholar
• Frydman J. Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 2001; 70: 603–647
   PubMed Web of Science ®Google Scholar
• Furlow J. D., Neff E. S. A developmental switch induced by thyroid hormone: Xenopus laevis metamorphosis. Trends Endocrinol Metab 2006; 17: 40–47
   PubMedGoogle Scholar
• Garcia-Cardenã G., Fan R., Shah V., Sorrentino R., Cirino G., Papapetropoulos A., Sessa W. C. Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature 1998; 392: 821–824
   PubMed Web of Science ®Google Scholar
• Gardner T. S., Cantor C. R., Collins J. J. Construction of a genetic toggle switch in Escherichia coli. Nature 2000; 403: 339–342
   PubMed Web of Science ®Google Scholar
• Gibson G., Wagner G. Canalization in evolutionary genetics: a stabilizing theory?. Bioessays 2000; 22: 372–380
   PubMedGoogle Scholar
• Gibson G., Dworkin I. Uncovering cryptic genetic variation. Nat Rev Genet 2004; 5: 681–690
   PubMed Web of Science ®Google Scholar
• Goldbeter A., Koshland D. E., Jr. Ultrasensitivity in biochemical systems controlled by covalent modification. Interplay between zero-order and multistep effects. J Biol Chem 1984; 259: 14441–14447
   PubMedGoogle Scholar
• Hansen T. F. Is modularity necessary for evolvability? Remarks on the relationship between pleiotropy and evolvability. Biosystems 2003; 69: 83–94
   PubMed Web of Science ®Google Scholar
• Helmbrecht K., Zeise E., Rensing L. Chaperones in cell cycle regulation and mitogenic signal transduction: a review. Cell Prolif 2000; 33: 341–365
   PubMed Web of Science ®Google Scholar
• Heyland A., Hodin J., Reitzel A. M. Hormone signaling in evolution and development: a non-model system approach. Bioessays 2005; 27: 64–75
   PubMedGoogle Scholar
• Holley S. J., Yamamoto K. R. A role for Hsp90 in retinoid receptor signal transduction. Mol Biol Cell 1995; 6: 1833–1842
   PubMedGoogle Scholar
• Houle D. Comparing evolvability and variability of quantitative traits. Genetics 1992; 130: 195–204
   PubMed Web of Science ®Google Scholar
• Lander A. D. Morpheus unbound: reimagining the morphogen gradient. Cell 2007; 128: 245–256
   PubMed Web of Science ®Google Scholar
• Leise E. M., Kempf S. C., Durham N. R., Gifondorwa D. J. Induction of metamorphosis in the marine gastropod Ilyanassa obsoleta: 5HT, NO and programmed cell death. Acta Biol Hung 2004; 55: 293–300
   PubMedGoogle Scholar
• Levine M., Davidson E. H. Gene regulatory networks for development. Proc Natl Acad Sci U S A 2005; 102: 4936–4942
   PubMed Web of Science ®Google Scholar
• Loubradou G., Bégueret J., Turcq B. A mutation in an HSP90 gene affects the sexual cycle and suppresses vegetative incompatibility in the fungus Podospora anserina. Genetics 1997; 147: 581–588
   PubMed Web of Science ®Google Scholar
• Loubradou G., Bégueret J., Turcq B. MOD-D, a Galpha subunit of the fungus Podospora anserina, is involved in both regulation of development and vegetative incompatibility. Genetics 1999; 152: 519–528
   PubMedGoogle Scholar
• Mackay T. F. The nature of quantitative genetic variation revisited: lessons from Drosophila bristles. Bioessays 1996; 18: 113–121
   PubMed Web of Science ®Google Scholar
• Maisnier-Patin S., Roth J. R., Fredriksson A., Nystrom T., Berg O. G., Andersson D. I. Genomic buffering mitigates the effects of deleterious mutations in bacteria. Nat Genet 2005; 37: 1376–1379
   PubMedGoogle Scholar
• Maloney A., Clarke P. A., Naaby-Hansen S., Stein R., Koopman J. O., Akpan A., Yang A., Zvelebil M., Cramer R., Stimson L., et al. Gene and protein expression profiling of human ovarian cancer cells treated with the heat shock protein 90 inhibitor 17-allylamino-17-demethoxygeldanamycin. Cancer Res 2007; 67: 3239–3253
   PubMed Web of Science ®Google Scholar
• Masel J. Evolutionary capacitance may be favored by natural selection. Genetics 2005; 170: 1359–1371
   PubMedGoogle Scholar
• Meiklejohn C. D., Hartl D. L. A single mode of canalization. Trends in Ecology and Evolution 2002; 17: 468–473
   Web of Science ®Google Scholar
• Milton C. C., Ulane C. M., Rutherford S. Control of canalization and evolvability by Hsp90. PLoS ONE 2006; 1: e75, doi:10.1371/ journal.pone.0000075
   Google Scholar
• Milton C. C., Huynh B., Batterham P., Rutherford S. L., Hoffmann A. A. Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability. Proc Natl Acad Sci USA 2003; 100: 13396–13401
   PubMedGoogle Scholar
• Mitchell H. K., Petersen N. S. Developmental abnormalities in Drosophila induced by heat shock. Developmental Genetics 1982; 3: 91–102
   Google Scholar
• Morimoto R. I. Dynamic remodeling of transcription complexes by molecular chaperones. Cell 2002; 110: 281–284
   PubMedGoogle Scholar
• Moriyama E. N., Powell J. R. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol 1996; 13: 261–277
   PubMedGoogle Scholar
• Nichols S. A., Dirks W., Pearse J. S., King N. Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci USA 2006; 103: 12451–12456
   PubMed Web of Science ®Google Scholar
• Nollen E. A., Morimoto R. I. Chaperoning signaling pathways: molecular chaperones as stress-sensing ‘heat shock’ proteins. J Cell Sci 2002; 115: 2809–2816
   PubMed Web of Science ®Google Scholar
• O'Farrell P. H. Triggering the all-or-nothing switch into mitosis. Trends Cell Biol 2001; 11: 512–519
   PubMed Web of Science ®Google Scholar
• Partridge L., Barton N. H. Evolving evolvability. Nature 2000; 407: 457–458
   Google Scholar
• Picard D. Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci 2002; 59: 1640–1648
   PubMed Web of Science ®Google Scholar
• Pineiro R. Selection for canalization at two extra dorsocentral bristles in Drosophila melanogaster. J Hered 1992; 83: 49–55
   PubMedGoogle Scholar
• Pires-daSilva A., Sommer R. J. The evolution of signalling pathways in animal development. Nat Rev Genet 2003; 4: 39–49
   PubMedGoogle Scholar
• Pratt W. B., Toft D. O. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 1997; 18: 306–360
   PubMed Web of Science ®Google Scholar
• Queitsch C., Sangster T. A., Lindquist S. Hsp90 as a capacitor of phenotypic variation. Nature 2002; 417: 618–624
   PubMed Web of Science ®Google Scholar
• Radman M., Matic I., Taddei F. Evolution of evolvability. Ann N Y Acad Sci 1999; 870: 146–155
   PubMedGoogle Scholar
• Reis T., Edgar B. A. Negative regulation of dE2F1 by cyclin-dependent kinases controls cell cycle timing. Cell 2004; 117: 253–264
   PubMed Web of Science ®Google Scholar
• Rendel J. M. Canalisation and gene control. Logos Press; Academic Press, London 1967
   Google Scholar
• Richter K., Buchner J. Hsp90: chaperoning signal transduction. J Cell Physiol 2001; 188: 281–290
   PubMed Web of Science ®Google Scholar
• Riddiford L. M., Cherbas P., Truman J. W. Ecdysone receptors and their biological actions. Vitam Horm 2000; 60: 1–73
   PubMed Web of Science ®Google Scholar
• Roberts B., Davidson B., Macmaster G., Lockhart V., Ma E., Wallace S. S., Swalla B. J. A complement response may activate metamorphosis in the ascidian Boltenia villosa. Dev Genes Evol 2007; 217: 449–458
   PubMedGoogle Scholar
• Ruden D. M., Xiao L., Garfinkel M. D., Lu X. Hsp90 and environmental impacts on epigenetic states: a model for the trans-generational effects of diethylstibesterol on uterine development and cancer. Hum Mol Genet 2005; 14: R149–155, Spec No. 1
   Google Scholar
• Rutherford S., Knapp J. R., Csmerely P. Hsp90 and developmental networks. Molecular aspects of the stress response, P. Csmerely, L. Vigh. Landes Bioscience, London 2007
   Google Scholar
• Rutherford S. L. From genotype to phenotype: buffering mechanisms and the storage of genetic information. Bioessays 2000; 22: 1095–1105
   PubMedGoogle Scholar
• Rutherford S. L. Between genotype and phenotype: protein chaperones and evolvability. Nat Rev Genet 2003; 4: 263–274
   PubMedGoogle Scholar
• Rutherford S. L., Zuker C. S. Protein folding and the regulation of signaling pathways. Cell 1994; 79: 1129–1132
   PubMed Web of Science ®Google Scholar
• Rutherford S. L., Lindquist S. Hsp90 as a capacitor for morphological evolution. Nature 1998; 396: 336–342
   PubMed Web of Science ®Google Scholar
• Rutherford S. L., Henikoff S. Quantitative epigenetics. Nat Genet 2003; 33: 6–8
   PubMedGoogle Scholar
• Modularity in development and evolution, G. Schlosser, G. P. Wagner. University of Chicago Press, Chicago 2004
   Google Scholar
• Schmalhausen I. I. Factors of evolution: the theory of stabilizing selection. University of Chicago Press, Chicago 1986
   Google Scholar
• Strathmann R., Eernisse D. What molecular phylogenies tell us about the evolution of larval forms. Am Zool 1994; 34: 502–512
   Google Scholar
• Swalla B. J. Building divergent body plans with similar genetic pathways. Heredity 2006; 97: 235–243
   PubMedGoogle Scholar
• van der Straten A., Rommel C., Dickson B., Hafen E. The heat shock protein 83 (Hsp83) is required for Raf-mediated signalling in Drosophila. Embo J 1997; 16: 1961–1969
   PubMed Web of Science ®Google Scholar
• Volfson D., Marciniak J., Blake W. J., Ostroff N., Tsimring L. S., Hasty J. Origins of extrinsic variability in eukaryotic gene expression. Nature 2006; 439: 861–864
   PubMed Web of Science ®Google Scholar
• von Dassow G., Meir E., Munro E. M., Odell G. M. The segment polarity network is a robust developmental module. Nature 2000; 406: 188–192
   PubMed Web of Science ®Google Scholar
• Waddington C. Canalization of development and the inheritance of acquired characters. Nature 1942; 150: 563
   Google Scholar
• Waddington C. H. Genetic assimilation of an acquired character. Evolution 1953; 7: 118–126
   Web of Science ®Google Scholar
• Waddington C. H. The strategy of the genes; a discussion of some aspects of theroetical biology. Macmillan, New York 1957
   Google Scholar
• Waddington C. H. Experiments on canalizing selection. Genet Research 1960; 1: 140–150
   Web of Science ®Google Scholar
• Wagner G. P., Altenberg L. Complex adaptations and the evolution of evolvability. Evolution 1996; 50: 967–976
   PubMed Web of Science ®Google Scholar
• Wagner G. P., Chiu C. H., Hansen T. F. Is Hsp90 a regulator of evolvability?. J Exp Zool 1999; 285: 116–118
   PubMedGoogle Scholar
• Wiesgigl M., Clos J. Heat shock protein 90 homeostasis controls stage differentiation in Leishmania donovani. Mol Biol Cell 2001; 12: 3307–3316
   PubMed Web of Science ®Google Scholar
• Wright S. An analysis of variability in number of digits in an inbred strain of guinea pigs. Genetics 1934; 19: 506–536
   PubMedGoogle Scholar
• Yang A. S. Modularity, evolvability, and adaptive radiations: a comparison of the hemi- and holometabolous insects. Evol Dev 2001; 3: 59–72
   PubMed Web of Science ®Google Scholar
• Yeyati P. L., Bancewicz R. M., Maule J., van Heyningen V. Hsp90 selectively modulates phenotype in vertebrate development. PLoS Genet 2007; 3: e43
   PubMed Web of Science ®Google Scholar
• Zhao R., Davey M., Hsu Y. C., Kaplanek P., Tong A., Parsons A. B., Krogan N., Cagney G., Mai D., Greenblatt J., et al. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 2005; 120: 715–727
   PubMed Web of Science ®Google Scholar
• Zou J., Guo Y., Guettouche T., Smith D. F., Voellmy R. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 1998; 94: 471–480
   PubMed Web of Science ®Google Scholar