Diversity in the origins of proteostasis networks-a driver for protein function in evolution

Nature Reviews Molecular Cell Biology

Volumn 14, Issue 4, 2013, Pages 237-248

  Powers, Evan T ^a   Balch, William E ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; CHAPERONE; CHAPERONIN CONTAINING TCP1; GLUCOSE REGULATED PROTEIN 78; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 100; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; PROTEOME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SMALL HEAT SHOCK PROTEIN; THERMOSOME; TRANSCRIPTION FACTOR FOXO;

ARABIDOPSIS; ARCHAEON; CELL AGING; CELL STRUCTURE; CELL SURVIVAL; CHRONIC OBSTRUCTIVE LUNG DISEASE; DEACETYLATION; DROSOPHILA MELANOGASTER; ESCHERICHIA COLI; EUKARYOTE; HEAT SHOCK RESPONSE; HISTONE ACETYLATION; HYDROGEN BOND; ISOMERIZATION; LAST COMMON ANCESTOR; MOLECULAR EVOLUTION; MUSCLE INJURY; MYCOPLASMA; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN INTERACTION; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; SMOKING; UNFOLDED PROTEIN RESPONSE;

ANIMALS; EVOLUTION, MOLECULAR; GENETIC VARIATION; HOMEOSTASIS; HUMANS; PROTEIN FOLDING; PROTEINS; PROTEOME; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

EUKARYOTA;

EID: 84875461582     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3542     Document Type: Review

References (141)

1. Anfinsen, C. B. Principles that govern the folding of protein chains. Science 181, 223-230 (1973).
2. Balch, W. E., Morimoto, R. I., Dillin, A. & Kelly, J. W. Adapting proteostasis for disease intervention. Science 319, 916-919 (2008). (Pubitemid 351263754)
3. Gidalevitz, T., Prahlad, V. & Morimoto, R. I. The stress of protein misfolding: from single cells to multicellular organisms. Cold Spring Harb. Perspect. Biol. 3, a009704 (2011).
4. Darwin, C. The Origin of Species. (1867).
5. Tokuriki, N. & Tawfik, D. S. Stability effects of mutations and protein evolvability. Curr. Opin. Struct. Biol. 19, 596-604 (2009).
6. Lindquist, S. Protein folding sculpting evolutionary change. Cold Spring Harb. Symp. Quant. Biol. 74, 103-108 (2009).
7. Broadley, S. A. & Hartl, F. U. The role of molecular chaperones in human misfolding diseases. FEBS Lett. 583, 2647-2653 (2009).
8. Powers, E. T., Morimoto, R. I., Dillin, A., Kelly, J. W. & Balch, W. E. Biological and chemical approaches to diseases of proteostasis deficiency. Annu. Rev. Biochem. 78, 959-991 (2009).
9. Douglas, P. M. & Dillin, A. Protein homeostasis and aging in neurodegeneration. J. Cell Biol. 190, 719-729 (2010).
10. Voisine, C., Pedersen, J. S. & Morimoto, R. I. Chaperone networks: tipping the balance in protein folding diseases. Neurobiol. Dis. 40, 12-20 (2010).
11. Lindquist, S. L. & Kelly, J. W. Chemical and biological approaches for adapting proteostasis to ameliorate protein misfolding and aggregation diseases: progress and prognosis. Cold Spring Harb. Perspect. Biol. 3, a004507 (2011).
12. Hutt, D. M. & Balch, W. E. Expanding proteostasis by membrane trafficking networks. Cold Spring Harb. Perspect. Biol. 19 Feb 2013 (doi:10.1101/cshperspect.a013383).
13. Hartl, F. U., Bracher, A. & Hayer-Hartl, M. Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332 (2011).
14. Taipale, M., Jarosz, D. F. & Lindquist, S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nature Rev. Mol. Cell Biol. 11, 515-528 (2010).
15. Chen, B., Retzlaff, M., Roos, T. & Frydman, J. Cellular strategies of protein quality control. Cold Spring Harb. Perspect. Biol. 3, a004374 (2011).
16. Kaganovich, D., Kopito, R. & Frydman, J. Misfolded proteins partition between two distinct quality control compartments. Nature 454, 1088-1095 (2008).
17. Tyedmers, J., Mogk, A. & Bukau, B. Cellular strategies for controlling protein aggregation. Nature Rev. Mol. Cell Biol. 11, 777-788 (2010).
18. Finley, D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78, 477-513 (2009).
19. Watts, C. The endosome-lysosome pathway and information generation in the immune system. Biochim. Biophys. Acta 1824, 14-21 (2012).
20. Yang, Z. & Klionsky, D. J. Mammalian autophagy: core molecular machinery and signaling regulation. Curr. Opin. Cell Biol. 22, 124-131 (2010).
21. Rubinsztein, D. C., Shpilka, T. & Elazar, Z. Mechanisms of autophagosome biogenesis. Curr. Biol. 22, R29-R34 (2012).
22. Muller, S., Dennemarker, J. & Reinheckel, T. Specific functions of lysosomal proteases in endocytic and autophagic pathways. Biochim. Biophys. Acta 1824, 34-43 (2012).
23. Lee, J., Giordano, S. & Zhang, J. Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem. J. 441, 523-540 (2012).
24. Lamark, T. & Johansen, T. Aggrephagy: selective disposal of protein aggregates by macroautophagy. Int. J. Cell Biol. 2012, 736905 (2012).
25. Kaushik, S. & Cuervo, A. M. Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol. 22, 407-417 (2012).
26. Husnjak, K. & Dikic, I. Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 81, 291-322 (2012).
27. Tokuriki, N. & Tawfik, D. S. Protein dynamism and evolvability. Science 324, 203-207 (2009).
28. Kikis, E. A., Gidalevitz, T. & Morimoto, R. I. Protein homeostasis in models of aging and age-related conformational disease. Adv. Exp. Med. Biol. 694, 138-159 (2010).
29. Fox, G. E. et al. The phylogeny of prokaryotes. Science 209, 457-463 (1980). (Pubitemid 10022749)
30. Balch, W. E., Magrum, L. J., Fox, G. E., Wolfe, R. S. & Woese, C. R. An ancient divergence among the bacteria. J. Mol. Evol. 9, 305-311 (1977). (Pubitemid 8163846)
31. Darwin, C. The Voyage of the Beagle. (1856).
32. Roberts, E., Sethi, A., Montoya, J., Woese, C. R. & Luthey-Schulten, Z. Molecular signatures of ribosomal evolution. Proc. Natl Acad. Sci. USA 105, 13953-13958 (2008).
33. Vetsigian, K., Woese, C. & Goldenfeld, N. Collective evolution and the genetic code. Proc. Natl Acad. Sci. USA 103, 10696-10701 (2006). (Pubitemid 44078039)
34. Horwich, A. L., Fenton, W. A., Chapman, E. & Farr, G. W. Two families of chaperonin: physiology and mechanism. Annu. Rev. Cell Dev. Biol. 23, 115-145 (2007).
35. Margittai, E. & Sitia, R. Oxidative protein folding in the secretory pathway and redox signaling across compartments and cells. Traffic 12, 1-8 (2011).
36. Vilchez, D. et al. Increased proteasome activity in human embryonic stem cells is regulated by PSMD11. Nature 489, 304-308 (2012).
37. Hutt, D. M., Powers, E. T. & Balch, W. E. The proteostasis boundary in misfolding diseases of membrane traffic. FEBS Lett. 583, 2639-2646 (2009).
38. Powers, E. T. & Balch, W. E. Protein folding: protection from the outside. Nature 471, 42-43 (2011).
39. Morimoto, R. I. The heat shock response: systems biology of proteotoxic stress in aging and disease. Cold Spring Harb. Symp. Quant. Biol. 76, 91-99 (2011).
40. Ong, D. S. & Kelly, J. W. Chemical and/or biological therapeutic strategies to ameliorate protein misfolding diseases. Curr. Opin. Cell Biol. 23, 231-238 (2011).
41. Pace, C. N. et al. Contribution of hydrophobic interactions to protein stability. J. Mol. Biol. 408, 514-528 (2011).
42. Bolen, D. W. & Rose, G. D. Structure and energetics of the hydrogen-bonded backbone in protein folding. Annu. Rev. Biochem. 77, 339-362 (2008).
43. Bartlett, G. J. Choudhary, A., Raines, R. T. & Woolfson, D. N. n → π* interactions in proteins. Nature Chem. Biol. 6, 615-620 (2010).
44. Goldberg, A. L. Protein degradation and protection against misfolded or damaged proteins. Nature 426, 895-899 (2003). (Pubitemid 38056882)
45. Chiti, F. & Dobson, C. M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366 (2006). (Pubitemid 44118036)
46. Kelly, J. W. The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr. Opin. Struct. Biol. 8, 101-106 (1998). (Pubitemid 28107921)
47. Ghosh, K. & Dill, K. Cellular proteomes have broad distributions of protein stability. Biophys. J. 99, 3996-4002 (2010).
48. Kultz, D. Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function. J. Exp. Biol. 206, 3119-3124 (2003). (Pubitemid 37181411)
49. Akerfelt, M., Morimoto, R. I. & Sistonen, L. Heat shock factors: integrators of cell stress, development and lifespan. Nature Rev. Mol. Cell Biol. 11, 545-555 (2010).
50. Pellegrino, M. W., Nargund, A. M. & Haynes, C. M. Signaling the mitochondrial unfolded protein response. Biochim Biophys Acta 1833, 410-416 (2012).
51. Nordhues, A., Miller, S. M., Muhlhaus, T. & Schroda, M. New insights into the roles of molecular chaperones in Chlamydomonas and Volvox. Int. Rev. Cell. Mol. Biol. 285, 75-113 (2010).
52. Kultz, D. Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 67, 225-257 (2005). (Pubitemid 40404492)
53. Chen, B., Zhong, D. & Monteiro, A. Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms. BMC Genomics 7, 156 (2006).
54. Haynes, C. M. & Ron, D. The mitochondrial UPR-protecting organelle protein homeostasis. J. Cell Sci. 123, 3849-3855 (2010).
55. Rudiger, S., Germeroth, L., Schneider-Mergener, J. & Bukau, B. Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J. 16, 1501-1507 (1997). (Pubitemid 27151945)
56. Blond-Elguindi, S. et al. Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75, 717-128 (1993).
57. Wang, Z., Feng, H., Landry, S. J., Maxwell, J. & Gierasch, L. M. Basis of substrate binding by the chaperonin GroEL. Biochemistry 38, 12537-12546 (1999).
58. Scheibel, T., Weikl, T. & Buchner, J. Two chaperone sites in Hsp90 differing in substrate specificity and ATP dependence. Proc. Natl Acad. Sci. USA 95, 1495-1499 (1998). (Pubitemid 28103420)
59. Genevaux, P., Georgopoulos, C. & Kelley, W. L. The Hsp70 chaperone machines of Escherichia coli: a paradigm for the repartition of chaperone functions. Mol. Microbiol. 66, 840-857 (2007). (Pubitemid 350050417)
60. Brocchieri, L. Conway de Macario, E. & Macario, A. J. hsp70 genes in the human genome: conservation and differentiation patterns predict a wide array of overlapping and specialized functions. BMC Evol. Biol. 8, 19 (2008).
61. Chen, B., Piel, W. H., Gui, L., Bruford, E. & Monteiro, A. The HSP90 family of genes in the human genome: insights into their divergence and evolution. Genomics 86, 627-637 (2005). (Pubitemid 41752943)
62. Sreedhar, A. S., Kalmar, E., Csermely, P. & Shen, Y. F. Hsp90 isoforms: functions, expression and clinical importance. FEBS Lett. 562, 11-15 (2004). (Pubitemid 38388440)
63. Chen, C. Y. & Balch, W. E. The Hsp90 chaperone complex regulates GDI-dependent Rab recycling. Mol. Biol. Cell 17, 3494-3507 (2006). (Pubitemid 44156443)
64. Sakisaka, T., Meerlo, T., Matteson, J., Plutner, H. & Balch, W. E. Rab-αGDI activity is regulated by a Hsp90 chaperone complex. EMBO J. 21, 6125-6135 (2002). (Pubitemid 35415329)
65. Walter, P. & Ron, D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081-1086 (2011).
66. Ostrovsky, O., Eletto, D., Makarewich, C., Barton, E. R. & Argon, Y. Glucose regulated protein 94 is required for muscle differentiation through its control of the autocrine production of insulin-like growth factors. Biochim. Biophys. Acta 1803, 333-341 (2010).
67. Weiss, C., Bonshtien, A., Farchi-Pisanty, O., Vitlin, A. & Azem, A. Cpn20: siamese twins of the chaperonin world. Plant Mol. Biol. 69, 227-238 (2009).
68. Peltier, J. B. et al. The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol. Cell Proteom. 5, 114-133 (2006).
69. Peng, L. et al. A chaperonin subunit with unique structures is essential for folding of a specific substrate. PLoS Biol. 9, e1001040 (2011).
70. Brewer, J. W. & Hendershot, L. M. Building an antibody factory: a job for the unfolded protein response. Nature Immunol. 6, 23-29 (2005). (Pubitemid 40136692)
71. Back, S. H., Kang, S. W., Han, J. & Chung, H. T. Endoplasmic reticulum stress in the β-cell pathogenesis of type 2 diabetes. Exp. Diabetes Res. 2012, 618396 (2012).
72. Prahlad, V., Cornelius, T. & Morimoto, R. I. Regulation of the cellular heat shock response in Caenorhabditis elegans by thermosensory neurons. Science 320, 811-814 (2008). (Pubitemid 351929633)
73. Bouchecareilh, M. & Balch, W. E. Proteostasis, an emerging therapeutic paradigm for managing inflammatory airway stress disease. Curr. Mol. Med. 12, 815-826 (2012).
74. Demasi, M. & Laurindo, F. R. Physiological and pathological pole of the ubiquitin-proteasome system in the vascular smooth muscle cell. Cardiovasc. Res. 95, 183-193 (2012).
75. Altun, M. et al. Muscle wasting in aged, sarcopenic rats is associated with enhanced activity of the ubiquitin proteasome pathway. J. Biol. Chem. 285, 39597-39608 (2010).
76. Lund, P. A. Multiple chaperonins in bacteria-why so many? FEMS Microbiol. Rev. 33, 785-800 (2009).
77. Williams, T. A. & Fares, M. A. The effect of chaperonin buffering on protein evolution. Genome Biol. Evol. 2, 609-619 (2010).
78. Fujiwara, K., Ishihama, Y., Nakahigashi, K., Soga, T. & Taguchi, H. A systematic survey of in vivo obligate chaperonin-dependent substrates. EMBO J. 29, 1552-1564 (2010).
79. Macario, A. J., Brocchieri, L., Shenoy, A. R. & Conway de Macario, E. Evolution of a protein-folding machine: genomic and evolutionary analyses reveal three lineages of the archaeal hsp70(dnaK) gene. J. Mol. Evol. 63, 74-86 (2006). (Pubitemid 43992006)
80. Vorderwulbecke, S. et al. Low temperature or GroEL/ES overproduction permits growth of Escherichia coli cells lacking trigger factor and DnaK. FEBS Lett. 559, 181-187 (2004). (Pubitemid 38186725)
81. Sawle, L. & Ghosh, K. How do thermophilic proteins and proteomes withstand high temperature? Biophys. J. 101, 217-227 (2011).
82. Richter, K., Haslbeck, M. & Buchner, J. The heat shock response: life on the verge of death. Mol. Cell 40, 253-266 (2010).
83. Pysz, M. A. et al. Transcriptional analysis of dynamic heat-shock response by the hyperthermophilic bacterium Thermotoga maritima. Extremophiles 8, 209-217 (2004). (Pubitemid 40876326)
84. Boonyaratanakornkit, B. B., Miao, L. Y. & Clark, D. S. Transcriptional responses of the deep-sea hyperthermophile Methanocaldococcus jannaschii under shifting extremes of temperature and pressure. Extremophiles 11, 495-503 (2007). (Pubitemid 46742133)
85. Bosch, T. C., Krylow, S. M., Bode, H. R. & Steele, R. E. Thermotolerance and synthesis of heat shock proteins: these responses are present in Hydra attenuata but absent in Hydra oligactis. Proc. Natl Acad. Sci. USA 85, 7927-7931 (1988).
86. Clark, M. S. & Peck, L. S. HSP70 heat shock proteins and environmental stress in antarctic marine organisms: a mini-review. Mar. Genom. 2, 11-18 (2009).
87. Bussieres, N. & Granger, R. J. Estimation of water temperature of large lakes in cold climate regions during the period of strong coupling between water and air temperature fluctuations. J. Atmospher. Ocean. Technol. 24, 285-296 (2007). (Pubitemid 46388887)
88. McCarty, J. S. & Walker, G. C. DnaK as a thermometer: threonine-199 is site of autophosphorylation and is critical for ATPase activity. Proc. Natl Acad. Sci. USA 88, 9513-9517 (1991). (Pubitemid 21915661)
89. Klostermeier, D., Seidel, R. & Reinstein, J. Functional properties of the molecular chaperone DnaK from Thermus thermophilus. J. Mol. Biol. 279, 841-853 (1998). (Pubitemid 28284699)
90. Place, S. P. & Hofmann, G. E. Comparison of Hsc70 orthologs from polar and temperate notothenioid fishes: differences in prevention of aggregation and refolding of denatured proteins. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R1195-R1202 (2005). (Pubitemid 40593702)
91. Tomanek, L. Variation in the heat shock response and its implication for predicting the effect of global climate change on species' biogeographical distribution ranges and metabolic costs. J. Exp. Biol. 213, 971-979 (2010).
92. Gidalevitz, T., Krupinski, T., Garcia, S. & Morimoto, R. I. Destabilizing protein polymorphisms in the genetic background direct phenotypic expression of mutant SOD1 toxicity. PLoS Genet. 5, e1000399 (2009).
93. Brennecke, T., Gellner, K. & Bosch, T. C. The lack of a stress response in Hydra oligactis is due to reduced hsp70 mRNA stability. Eur. J. Biochem. 255, 703-709 (1998). (Pubitemid 28372306)
94. Tian, S., Haney, R. A. & Feder, M. E. Phylogeny disambiguates the evolution of heat-shock cis-regulatory elements in Drosophila. PLoS ONE 5, e10669 (2010).
95. Garbuz, D. G. et al. Functional organization of hsp70 cluster in camel (Camelus dromedarius) and other mammals. PLoS ONE 6, e27205 (2011).
96. Garbuz, D. G. et al. Organization and evolution of hsp70 clusters strikingly differ in two species of Stratiomyidae (Diptera) inhabiting thermally contrasting environments. BMC Evol. Biol. 11, 74 (2011).
97. Keller, I. & Seehausen, O. Thermal adaptation and ecological speciation. Mol. Ecol. 21, 782-799 (2012).
98. Rashkovetsky, E. et al. Adaptive differentiation of thermotolerance in Drosophila along a microclimatic gradient. Hered. (Edinb.) 96, 353-359 (2006). (Pubitemid 43670398)
99. Michalak, P. et al. Genetic evidence for adaptation-driven incipient speciation of Drosophila melanogaster along a microclimatic contrast in "Evolution Canyon", Israel. Proc. Natl Acad. Sci. USA 98, 13195-13200 (2001). (Pubitemid 33051339)
100. Carmel, J., Rashkovetsky, E., Nevo, E. & Korol, A. Differential expression of small heat shock protein genes Hsp23 and Hsp40, and heat shock gene Hsr-ω in fruit flies (Drosophila melanogaster) along a microclimatic gradient. J. Hered. 102, 593-603 (2011).
101. Walser, J. C., Chen, B. & Feder, M. E. Heat-shock promoters: targets for evolution by P transposable elements in Drosophila. PLoS Genet. 2, e165 (2006).
102. Jarosz, D. F. & Lindquist, S. Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science 330, 1820-1824 (2010).
103. Jarosz, D. F., Taipale, M. & Lindquist, S. Protein homeostasis and the phenotypic manifestation of genetic diversity: principles and mechanisms. Annu. Rev. Genet. 44, 189-216 (2010).
104. Dai, C., Whitesell, L., Rogers, A. B. & Lindquist, S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 130, 1005-1018 (2007). (Pubitemid 47410269)
105. Trepel, J., Mollapour, M., Giaccone, G. & Neckers, L. Targeting the dynamic HSP90 complex in cancer. Nature Rev. Cancer 10, 537-549 (2010).
106. Santagata, S. et al. Using the heat-shock response to discover anticancer compounds that target protein homeostasis. ACS Chem. Biol. 7, 340-349 (2012).
107. Mendillo, M. L. et al. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 150, 549-562 (2012).
108. Geller, R., Taguwa, S. & Frydman, J. Broad action of Hsp90 as a host chaperone required for viral replication. Biochim. Biophys. Acta 1823, 698-706 (2012).
109. Tokuriki, N., Oldfield, C. J., Uversky, V. N., Berezovsky, I. N. & Tawfik, D. S. Do viral proteins possess unique biophysical features? Trends Biochem. Sci. 34, 53-59 (2009).
110. Tokuriki, N. & Tawfik, D. S. Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 459, 668-673 (2009).
111. Specchia, V. et al. Hsp90 prevents phenotypic variation by suppressing the mutagenic activity of transposons. Nature 463, 662-665 (2010).
112. Abdelhakim, A. H., Oakes, E. C., Sauer, R. T. & Baker, T. A. Unique contacts direct high-priority recognition of the tetrameric transposase-DNA complex by the AAA+ unfoldase ClpX. Mol. Cell 30, 39-50 (2008). (Pubitemid 351470146)
113. Tariq, M., Nussbaumer, U., Chen, Y., Beisel, C. & Paro, R. Trithorax requires Hsp90 for maintenance of active chromatin at sites of gene expression. Proc. Natl Acad. Sci. USA 106, 1157-1162 (2009).
114. DeZwaan, D. C. & Freeman, B. C. HSP90 manages the ends. Trends Biochem. Sci. 35, 384-391 (2010).
115. Hageman, J. et al. A DNAJB chaperone subfamily with HDAC-dependent activities suppresses toxic protein aggregation. Mol. Cell 37, 355-369 (2010).
116. Marinova, Z. et al. Valproic acid induces functional heat-shock protein 70 via class I histone deacetylase inhibition in cortical neurons: a potential role of Sp1 acetylation. J. Neurochem. 111, 976-987 (2009).
117. Boyault, C., Sadoul, K., Pabion, M. & Khochbin, S. HDAC6, at the crossroads between cytoskeleton and cell signaling by acetylation and ubiquitination. Oncogene 26, 5468-5476 (2007). (Pubitemid 47255928)
118. Westerheide, S. D. et al. Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323, 1063-1066 (2009).
119. Morimoto, R. I. & Cuervo, A. M. Protein homeostasis and aging: taking care of proteins from the cradle to the grave. J. Gerontol. A Biol. Sci. Med. Sci. 64, 167-170 (2009).
120. Boyault, C. et al. HDAC6 controls major cell response pathways to cytotoxic accumulation of protein aggregates. Genes Dev. 21, 2172-2181 (2007). (Pubitemid 47360839)
121. Araki, K. & Inaba, K. Structure, mechanism, and evolution of Ero1 family enzymes. Antioxid. Redox Signal 16, 790-799 (2012).
122. Braakman, I. & Bulleid, N. J. Protein folding and modification in the mammalian endoplasmic reticulum. Annu. Rev. Biochem. 80, 71-99 (2011).
123. Giudice, A., Arra, C. & Turco, M. C. Review of molecular mechanisms involved in the activation of the Nrf2-ARE signaling pathway by chemopreventive agents. Methods Mol. Biol. 647, 37-74 (2010).
124. Rabinowitz, J. D. & White, E. Autophagy and metabolism. Science 330, 1344-1348 (2010).
125. Carrano, A. C., Liu, Z., Dillin, A. & Hunter, T. A conserved ubiquitination pathway determines longevity in response to diet restriction. Nature 460, 396-399 (2009).
126. Fadini, G. P., Ceolotto, G., Pagnin, E., de Kreutzenberg, S. & Avogaro, A. At the crossroads of longevity and metabolism: the metabolic syndrome and lifespan determinant pathways. Aging Cell 10, 10-17 (2011).
127. Piper, R. C. & Lehner, P. J. Endosomal transport via ubiquitination. Trends Cell Biol. 21, 647-655 (2011).
128. Weissman, A. M., Shabek, N. & Ciechanover, A. The predator becomes the prey: regulating the ubiquitin system by ubiquitylation and degradation. Nature Rev. Mol. Cell Biol. 12, 605-620 (2011).
129. Durieux, J., Wolff, S. & Dillin, A. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 144, 79-91 (2011).
130. Balch, W. E., Roth, D. M. & Hutt, D. M. Emergent properties of proteostasis in managing cystic fibrosis. Cold Spring Harb. Perspect. Biol. 3, a004499 (2011).
131. Westermark, P., Andersson, A. & Westermark, G. T. Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiol. Rev. 91, 795-826 (2011).
132. Back, S. H. & Kaufman, R. J. Endoplasmic reticulum stress and type 2 diabetes. Annu. Rev. Biochem. 81, 767-793 (2012).
133. Whitesell, L. & Lindquist, S. Inhibiting the transcription factor HSF1 as an anticancer strategy. Expert Opin. Ther. Targets 13, 469-478 (2009).
134. Vinciguerra, M., Musaro, A. & Rosenthal, N. Regulation of muscle atrophy in aging and disease. Adv. Exp. Med. Biol. 694, 211-233 (2010).
135. Musial, K. & Zwolinska, D. Heat shock proteins in chronic kidney disease. Pediatr. Nephrol. 26, 1031-1037 (2011).
136. Wu, J. & Kaufman, R. J. From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ. 13, 374-384 (2006).
137. Wang, M. & Caetano-Anolles, G. The evolutionary mechanics of domain organization in proteomes and the rise of modularity in the protein world. Structure 17, 66-78 (2009).
138. Marsh, J. A. & Teichmann, S. A. How do proteins gain new domains? Genome Biol. 11, 126 (2010).
139. Dekker, C., Willison, K. R. & Taylor, W. R. On the evolutionary origin of the chaperonins. Proteins 79, 1172-1192 (2011).
140. Sharma, S. K., De los Rios, P., Christen, P., Lustig, A. & Goloubinoff, P. The kinetic parameters and energy cost of the Hsp70 chaperone as a polypeptide unfoldase. Nature Chem. Biol. 6, 914-920 (2010).
141. Doyle, S. M. & Wickner, S. Hsp104 and ClpB: protein disaggregating machines. Trends Biochem. Sci. 34, 40-48 (2009).