Under cover: Causes, effects and implications of Hsp90-mediated genetic capacitance

BioEssays

Volumn 26, Issue 4, 2004, Pages 348-362

  Sangster, Todd A ^a,b   Lindquist, Susan ^a   Queitsch, Christine ^c  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN 90; REGULATOR PROTEIN;

CHEMICAL ANALYSIS; ENVIRONMENTAL EXPOSURE; EPIGENETICS; EVOLUTION; EVOLUTIONARY ADAPTATION; GENE SILENCING; GENETIC ANALYSIS; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOME; GENOTYPE PHENOTYPE CORRELATION; PHENOTYPE; PROTEIN FOLDING; QUALITY CONTROL; REVIEW; SOLID TUMOR;

ANIMALS; ARABIDOPSIS; DROSOPHILA MELANOGASTER; ENVIRONMENT; GENOTYPE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MODELS, BIOLOGICAL; MODELS, GENETIC; MOLECULAR CHAPERONES; NEOPLASMS; PHENOTYPE; POLYMORPHISM, GENETIC; TEMPERATURE; VARIATION (GENETICS);

EID: 1842782331     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.20020     Document Type: Review

References (108)

1. Waddington CH. 1942. Canalization of development and the inheritance of acquired characters. Nature 150:563-565.
2. Siegal ML, Bergman A. 2002. Waddingtor's canalization revisited: developmental stability and evolution. Proc Natl Acad Sci USA 99:10528-10532.
3. Rutherford SL, Lindquist S. 1998. Hsp90 as a capacitor for morphological evolution. Nature 396:336-342.
4. Queitsch C, Sangster TA, Lindquist S. 2002. Hsp90 as a capacitor of phenotypic variation. Nature 417:618-624.
5. Mayer MP, Bukau B. 1999. Molecular chaperones: the busy life of Hsp90. Curr Biol 9:R322-325.
6. Frydman J. 2001. Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70:603-647.
7. Haslbeck M. 2002. sHsps and their role in the chaperone network. Cell Mol Life Sci 59:1649-1657.
8. Pratt WB, Toft DO. 2003. Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med 228:111-133.
9. Sauer FG, Barnhart M, Choudhury D, Knight SD, Waksman G, Hultgren SJ. 2000. Chaperone-assisted pilus assembly and bacterial attachment. Curr Opin Struct Biol 10:548-556.
10. Pratt WB, Krishna P, Olsen LJ. 2001. Hsp90-binding immunophilins in plants the protein movers. Trends Plant Sci 6:54-58.
11. Buchner J. 1999. Hsp90 & Co. - a holding for folding. Trends Biochem Sci 24:136-141.
12. Picard D. 2002. Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci 59:1640-1648.
13. Young JC, Moarefi I, Hartl FU. 2001. Hsp90: a specialized but essential protein-folding tool. J Cell Biol 15:267-273.
14. Picard D, Khursheed B, Garabedian MJ, Fortin MG, Lindquist S, Yamamoto KR. 1990. Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 348:166-168.
15. Xu Y, Singer MA, Lindquist S. 1999. Maturation of the tyrosine kinase c-src as a kinase and as a substrate depends on the molecular chaperone Hsp90. Proc Natl Acad Sci USA 96:109-114.
16. Nathan DF, Vos MH, Lindquist S. 1997. In vivo functions of the Saccharomyces cerevisiae Hsp90 chaperone. Proc Natl Acad Sci USA 94:12949-12956.
17. Citri A, Alroy I, Lavi S, Rubin C, Xu W, Grammatikakis N, Patterson C, Neckers L, Fry DW, Yarden Y. 2002. Drug-induced ubiquitylation and degradation of ErbB receptor tyrosine kinases: implications for cancer therapy. Embo J 21:2407-2417.
18. Alonso-Blanco C, Peeters AJ, Koornneef M, Lister C, Dean C, van der Bosch N, Pot J, Kuiper MT. 1998. Development of an AFLP based linkage map of Ler, Col and Cvi Arabidopsis thaliana ecotypes and construction of a Ler/Cvi recombinant inbred line population. Plant J 14:259-271.
19. Bergman A, Siegal ML. 2003. Evolutionary capacitance as a general feature of complex gene networks. Nature 424:549-552.
20. Sollars V, Lu X, Xiao L, Wang X, Garfinkel MD, Ruden DM. 2003. Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution. Nat Genet 33:70-74.
21. Francis NJ, Kingston RE. 2001. Mechanisms of transcriptional memory. Nat Rev Mol Cell Biol 2:409-421.
22. Freeman BC, Yamamoto KR. 2002. Disassembly of transcriptional regulatory complexes by molecular chaperones. Science 296:2232-2235.
23. Fletcher TM, Xiao N, Mautino G, Baumann CT, Wolford R, Warren BS, Hager GL. 2002. ATP-dependent mobilization of the glucccorticoid receptor during chromatin remodeling. Mol Cell Biol 22:3255-3263.
24. Sangster TA, Queitsch C, Lindquist S. 2003. Hsp90 and chromatin: Where is the link? Cell Cycle 2:166-168.
25. Zou J, Guo Y, Guettouche T, Smith DF, Voellmy R. 1998. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1 Cell 94:471-480.
26. Duina AA, Kalton HM, Gaber RF. 1998. Requirement for Hsp90 and a CyP-40-type cyclophilin in negative regulation of the heat shock response. J Biol Chem 273:18974-18978.
27. Guo Y, Guettouche T, Fenna M, Boellmann F, Pratt WB, Toft DO, Smith DF, Voellmy R. 2001. Evidence for a mechanism of repression of heat shock factor 1 transcriptional activity by a multichaperone complex. J Biol Chem 276:45791-45799.
28. Young JC, Hoogenraad NJ, Hartl FU. 2003. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112:41-50.
29. Boudeau J, Deak M, Lawlor MA, Morrice NA, Alessi DR. 2003. Heat-shock protein 90 and Cdc37 interact with LKB1 and regulate its stability. Biochem J 370:849-857.
30. Alberti S, Demand J, Esser C, Emmerich N, Schild H, Hohfeld J. 2002. Ubiquitylation of BAG-1 suggests a novel regulatory mechanism during the sorting of chaperone substrates to the proteasome. J Biol Chem 277:45920-45927.
31. Cyr DM, Hohfeld J, Patterson C. 2002. Protein quality control: U-box-containing E3 ubiquitin ligases join the fold. Trends Biochem Sci 27:368-375.
32. Connell P, Ballinger CA, Jiang J, Wu Y, Thompson LJ, Hohfeld J, Patterson C. 2001. The co-chaperone CHIP regulates protein triage decisions mediated by heat-shock proteins. Nat Cell Biol 3:93-96.
33. Peng Z, Serino G, Deng XW. 2001. Molecular characterization of subunit 6 of the COP9 signalosome and its role in multifaceted developmental processes in Arabidopsis. Plant Cell 13:2393-2407.
34. Peng Z, Serino G, Deng XW. 2001. A role of Arabidopsis COP9 signalosome in multifaceted developmental processes revealed by the characterization of its subunit 3. Development 128:4277-4288.
35. Rudiger S, Germercth L, Schneider-Mergener J, Bukau B. 1997. Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. Embo J 16:1501-1507.
36. Flynn GC, Pohl J, Flocco MT, Rothman JE. 1991. Peptide-binding specificity of the molecular chaperone BiP. Nature 353:726-730.
37. Blond-Elguindi S, Cwirla SE, Dower WJ, Lipshutz RJ, Sprang SR, Sambrook JF, Gething MJ. 1993. Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75:717-728.
38. Gragerov A, Zeng L, Zhao X, Burkholder W, Gottesman ME. 1994. Specificity of DnaK-peptide binding. J Mol Biol 235:848-854.
39. Hartl FU, Hayer-Hartl M. 2002. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852-1858.
40. Borkovich KA, Farrelly FW, Finkelstein DB, Taulien J, Lindquist S. 1989. hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol Cell Biol 9:3919-3930.
41. Craig EA, Yan W, James P. 1999. Genetic dissection of the Hsp70 chaperone system of yeast In: Bukau B editor. Molecular chaperones and folding catalysts: regulation, cellular function and mechanisms. Amsterdam: Harwood Academic Publishers. p 139-162.
42. Roberts SP, Feder ME. 1999. Natural hyperthermia and expression of the heat shock protein Hsp70 affect developmental abnormalities in Drosophila melanogaster. Oecologia 121:323-329.
43. Bardwell JC, Craig EA. 1988. Ancient heat shock gene is dispensable. J Bacteriol 170:2977-2983.
44. Netzer WJ, Hartl FU. 1998. Protein folding in the cytosol: chaperonin-dependent and -independent mechanisms. Trends Biochem Sci 23:68-73.
45. Fares MA, Ruiz-Gonzalez MX, Moya A, Elena SF, Barrio E. 2002. Endosymbiotic bacteria: groEL buffers against deleterious mutations Nature 417:398.
46. Jenkins AJ, March JB, Oliver IR, Masters M. 1986. A DNA fragment containing the groE genes can suppress mutations in the Escherichia coli dnaA gene. Mol Gen Genet 202:446-454.
47. Fayet O, Louarn JM, Georgopoulos C. 1986. Suppression of the Escherichia coli dnaA46 mutation by amplification of the groES and groEL genes. Mol Gen Genet 202:435-445.
48. Cheng L, Hirst K, Piper PW. 1992. Authentic temperature-regulation of a heat shock gene inserted into yeast on a high copy number vector. Influences of overexpression of HSP90 protein on high temperature growth and thermotolerance. Biochim Biophys Acta 1132:26-34.
49. Sung DY, Guy CL. 2003. Physiological and molecular assessment of altered expression of hsc70-1 in Arabidopsis: Evidence for pleiotropic consequences. Plant Physiology 132:979-987.
50. Krebs RA, Feder ME. 1997. Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2:60-71.
51. Feder JH, Rossi JM, Solomon J, Solomon N, Lindquist S. 1992. The consequences of expressing hsp70 in Drosophila cells at normal temperatures. Genes Dev 6:1402-1413.
52. Kamal A, Thao L, Sensintaffar J, Zhang L, Boehm MF, Fritz LC, Burrows FJ. 2003. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425:407-410.
53. Welte MA, Tetrault JM, Dellavalle RP, Lindquist SL. 1993. A new method for manipulating transgenes: engineering heat tolerance in a complex, multicellular organism. Curr Biol 3:842-853.
54. Bustamante CD, Nielsen R, Sawyer SA, Olsen KM, Purugganan MD, Hartl DL. 2002. The cost of inbreeding in Arabidopsis Nature 416:531-534.
55. Krishna P, Gloor G. 2001. The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6:238-246.
56. Milioni D, Hatzopoulos P. 1997. Genomic organization of hsp90 gene family in Arabidopsis. Plant Mol Biol 35:955-961.
57. Partridge L, Barton NH. 2000. Evolving evolvability Nature 407:457-458.
58. Sniegowski PD, Gerrish PJ, Johnson T, Shaver A. 2000. The evolution of mutation rates: separating causes from consequences. Bioessays 22:1057-1066.
59. Rutherford SL. 2003. Between genotype and phenotype: protein chaperones and evolvability. Nat Rev Genet 4:263-274.
60. Masel J, Bergman A. 2003. The evolution of the evolvability properties of the yeast prion [PSI+]. Evolution 57:1498-1512.
61. Gould SJ, Lewontin RC. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B Biol Sci 205:581-598.
62. Queitsch C. 2001. Thermotolerance, buffering of genetic variation and developmental stability - different aspects of chaperone function in the plant Arabidopsis thaliana Thesis. Department of Molecular Genetics and Cell Biology. University of Chicago.
63. Petersen NS, Mitchell HK. 1987. The induction of a multiple wing hair phenocopy by heat shock in mutant heterozygotes. Dev Biol 121:335-341.
64. Wright S. 1931. Evolution of Mendelian populations. Genetics 16:97-159.
65. Hansen TF, Carter AJ, Chiu CH. 2000. Gene conversion may aid adaptive peak shifts. J Theor Biol 207:495-511.
66. Pigliucci M. 2001. Phenotypic plasticity: Beyond nature and nurture. Baltimore, MD: Johns Hopkins University Press.
67. Schlichting CD, Pigliucci M. 1998. Phenotypic evolution: A reaction norm perspective Sunderland, MA: Sinauer.
68. Waddington CH. 1953. Genetic assimilation of an acquired character. Evolution 7:118-126.
69. Waddington CH. 1956. Genetic assimilation of the bithorax phenotype. Evolution 10:1-13.
70. Kawecki TJ. 1995. Expression of genetic and environmental variation for life history characters on the usual and novel hosts in Callosobruchus maculatus (Coleoptera: Bruchidae) Heredity 75:70-76.
71. Guntrip J, Sibly RM, Holloway GJ. 1997. The effect of novel environment and sex on the additive genetic variation and covariation in and between emergence body weight and development period in the cowpea weevil. Callosobruchus maculatus (Coleoptera, Bruchidae). Heredity 78:158-165.
72. Imasheva AG, Moreteau B, David JR. 2000. Growth temperature and genetic variability of wing dimensions in Drosophila: opposite trends in two sibling species. Genet Res 76:237-247.
73. Bubliy OA, Loeschcke V. 2002. Effect of low stressful temperature on genetic variation of five quantitative traits in Drosophila melanogaster. Heredity 89:70-75.
74. Murphy PA, Giesel JT, Manlove MN. 1983. Temperature effects on life history variation in Drosophila simulans. Evolution 37:1181-1192.
75. Sgro CM, Hoffmann AA. 1998. Effects of stress combinations on the expression of additive genetic variation for fecundity in Drosophila melanogaster. Genet Res 72:13-18.
76. Rodriguez RL, Greenfield MD. 2003. Genetic variance and phenotypic plasticity in a component of female mate choice in an ultrasonic moth. Evolution 57:1304-1313.
77. Imasheva AG, Loeschcke V, Zhivotovsky LA, Lazebny OE. 1998. Stress temperatures and quantitative variation in Drosophila melanogaster. Heredity 81:246-253.
78. Beacham TD. 1987. Genotype-environment interactions in growth of chum salmon. Canadian Technical Report of Fisheries & Aquatic Sciences I-V:1-11.
79. Neyfakh AA, Hartl DL. 1993. Genetic control of the rate of embryonic development: Selection for faster development at elevated temperatures. Evolution 47:1625-1631.
80. Dorn LA, Pyle EH, Schmitt J. 2000. Plasticity to light cues and resources in Arabidopsis thaliana: testing for adaptive value and costs. Evolution 54:1982-1994.
81. Wiesgigl M, Clos J. 2001. Heat shock protein 90 homeostasis controls stage differentiation in Leishmania donovani. Mol Biol Cell 12:3307-3316.
82. Thoday JM. 1953. Balance, heterozygosity and developmental stability. Cold Spring Harb Symp Quant Biol 20:318-326.
83. Gibson G, Wagner G. 2000. Canalization in evolutionary genetics: a stabilizing theory? Bioessays 22:372-380.
84. Meiklejohn CD, Hartl DL. 2002. A single mode of canalization. Trends Ecol Evol 17:468-473.
85. Wilkins AS. 1997. Canalization: a molecular genetic perspective. Bioessays 19:257-262.
86. Whittle JRS. 1998. How is developmental stability sustained in the face of genetic variation? Int J Dev Biol 42:495-499.
87. Schmalhausen II. 1949. Factors of evolution: The theory of stabilizing selection. Chicago: University of Chicago Press
88. Gu Z, Steinmetz LM, Gu X, Scharfe C, Davis RW, Li WH. 2003. Role of duplicate genes in genetic robustness against null mutations. Nature 421:63-66.
89. Kawecki TJ. 2000. The evolution of genetic canalization under fluctuating selection. Evolution 54:1-12.
90. Eshel I, Matessi C. 1998. Canalization, genetic assimilation and pre-adaptation. A quantitative genetic model. Genetics 149:2119-2133.
91. Wagner A. 1996. Does evolutionary plasticity evolve? Evolution 50:1008-1023.
92. Wagner A. 2000. Robustness against mutations in genetic networks of yeast. Nat Genet 24:355-361.
93. Milton CC, Huynh B, Batterham P, Rutherford SL, Hoffmann AA. 2003. Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability. Proc Natl Acad Sci USA 100:13396-13401.
94. Reale D, Roff DA. 2003. Inbreeding, developmental stabilty, and canalization in the sand cricket Gryllus firmus. Evolution 57:597-605.
95. Davies AG, Game AY, Chen Z, Williams TJ, Goodall S, Yen JL, McKenzie JA, Batterham P. 1996. Scalloped wings is the Lucilia cuprina Notch homologue and a candidate for the modifier of fitness and asymmetry of diazinon resistance. Genetics 143:1321-1337.
96. Neckers L. 2002. Hsp90 inhibitors as novel cancer chemotherapeutic agents. Trends Mol Med 8:S55-S61.
97. Blagosklonny MV. 2002. Hsp-90-associated oncoproteins: multiple targets of geldanamycin and its analogs. Leukemia 16:455-462.
98. Chiosis G, Huezo H, Rosen N, Mimnaugh E, Whitesell L, Neckers L. 2003. 17AAG: low target binding affinity and potent cell activity-finding an explanation. Mol Cancer Ther 2:123-129.
99. Tomlinson IP, Roylance R, Houlston RS. 2001. Two hits revisited again. J Med Genet 38:81-85.
100. Plass C, Soloway PD. 2002. DNA methylaticn, imprinting and cancer. Eur J Hum Genet 10:6-16.
101. Tucker T, Friedman JM. 2002. Pathogenesis of hereditary tumors: beyond the "two-hit" hypothesis. Clin Genet 62:345-357.
102. Uehara Y, Hori M, Takeuchi T, Umezawa H. 1986. Phenotypic change from transformed to normal induced by benzoquinonoid ansamycins accompanies inactivation of p60src in rat kidney cells infected with Rous sarcoma virus. Mol Cell Biol 6:2198-2206.
103. Whitesell L, Mimnaugh EG, De Costa B, Myers CE, Neckers LM. 1994. Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc Natl Acad Sci USA 91:8324-8328.
104. Galis F. 1999. Why do almost all mammals have seven cervical vertebrae? Developmental constraints, Hox genes, and cancer. J Exp Zool 285:19-26.
105. Kishony R, Leibler S. 2003. Environmental stresses can alleviate the average deleterious effect of mutations. J Biol 2:14.
106. Georgiou G, Valax P. 1996. Expression of correctly folded proteins in Escherichia coli. Curr Opin Biotechnol 7:190-197.
107. Sharma M, Benharouga M, Hu W, Lukacs GL. 2001. Conformational and temperature-sensitive stability defects of the delta F508 cystic fibrosis transmembrane conductance regulator in post-endoplasmic reticulum compartments. J Biol Chem 276:8942-8950.
108. DePace AH, Weissman JS. 2002. Origins and kinetic consequences of diversity in Sup35 yeast prion fibers. Nat Struct Biol 9:389-396.