Advertisement

Thiol-Based Redox Signaling: Impacts on Molecular Chaperones and Cellular Proteostasis

  • Amy E. Ford
  • Kevin A. MoranoEmail author
Chapter
Part of the Heat Shock Proteins book series (HESP, volume 17)

Abstract

Signaling through protein cysteine residues to regulate diverse biological processes is widely conserved from bacterial to human cells. Differential cysteine reactivity enables cells to sense and respond to perturbations in the cellular redox environment, which may impact protein structure and activity. This chapter will focus on how redox signaling regulates components of the protein quality control network to mitigate proteotoxic stress caused by redox active compounds. While specifics of redox-based activation of the endoplasmic reticulum unfolded protein response and the cytoplasmic heat shock and oxidative stress responses differ, the presence of regulatory proteins containing reactive cysteines is a common feature. Moreover, several protein chaperones are reversibly regulated via cysteine switches that govern their ability to protect or refold damaged polypeptides. These responses are biologically indispensable, given the propensity of dysregulated cells to produce endogenous reactive oxygen species and the prevalence of thiol-reactive xenobiotics in the external environment.

Keywords

Chaperone Oxidative stress Proteostasis Reactive oxygen species Redox Signaling 

Abbreviations

CRD

cysteine-rich domain

Cys

cysteine

ER

endoplasmic reticulum

HMW

high molecular weight

HS

heat shock

HSP

heat shock protein

HSR

heat shock response

LMW

low molecular weight

NBD

nucleotide binding domain

NEF

nucleotide exchange factor

OS

oxidative stress

OSR

oxidative stress response

PDI

protein disulfide isomerase

PQC

protein quality control

Prx

peroxiredoxin

ROS

reactive oxygen species

SOH

sulfenic acid

TF

transcription factor

Ub

ubiquitin

UPR

unfolded protein response

Notes

Acknowledgements

Work in the authors’ laboratory was supported by NIH grant GM127287.

References

  1. Abravaya K, Myers MP, Murphy SP, Morimoto RI (1992) The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev 6:1153–1164PubMedCrossRefPubMedCentralGoogle Scholar
  2. Ahn SG, Thiele DJ (2003) Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev 17:516–528PubMedPubMedCentralCrossRefGoogle Scholar
  3. Arsène F, Tomoyasu T (2000) The heat shock response of Escherichia coli. Int J Food Microbiol 55:3–9PubMedCrossRefPubMedCentralGoogle Scholar
  4. Bankapalli K, Saladi SD, Awadia SS, Goswami AV, Samaddar M, D’Silva P (2015) Robust glyoxalase activity of Hsp31, a ThiJ/DJ-1/PfpI family member protein, is critical for oxidative stress resistance in Saccharomyces cerevisiae. J Biol Chem 290:26491–26507PubMedPubMedCentralCrossRefGoogle Scholar
  5. Barbirz S, Jakob U, Glocker MO (2000) Mass spectrometry unravels disulfide bond formation as the mechanism that activates a molecular chaperone. J Biol Chem 275:18759–18766PubMedCrossRefPubMedCentralGoogle Scholar
  6. Beck R, Verrax J, Gonze T et al (2009) Hsp90 cleavage by an oxidative stress leads to its client proteins degradation and cancer cell death. Biochem Pharmacol 77:375–383PubMedCrossRefPubMedCentralGoogle Scholar
  7. Bharadwaj S, Ali A, Ovsenek N (1999) Multiple components of the HSP90 chaperone complex function in regulation of heat shock factor 1 In vivo. Mol Cell Biol 19:8033–8041PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bhattacharyya S, Yu H, Mim C, Matouschek A (2014) Regulated protein turnover: snapshots of the proteasome in action. Nat Rev Mol Cell Biol 15:122–133PubMedPubMedCentralCrossRefGoogle Scholar
  9. Braakman I, Helenius J, Helenius A (1992) Manipulating disulfide bond formation and protein folding in the endoplasmic reticulum. EMBO J 11:1717–1722PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bracher A, Verghese J (2015) The nucleotide exchange factors of Hsp70 molecular chaperones. Subcell Biochem 78:1–33PubMedCrossRefPubMedCentralGoogle Scholar
  11. Brandes N, Reichmann D, Tienson H, Leichert LI, Jakob U (2011) Using quantitative redox proteomics to dissect the yeast redoxome. J Biol Chem 286:41893–41903PubMedPubMedCentralCrossRefGoogle Scholar
  12. Brandes N, Tienson H, Lindemann A, Vitvitsky V, Reichmann D, Banerjee R, Jakob U (2016) Time line of redox events in aging postmitotic cells. eLife 2:e00306CrossRefGoogle Scholar
  13. Cai H, Wang C-C, Tsou C-L (1994) Chaperone-like activity of protein disulfide isomerase in the refolding of a protein with no disulfide bonds. J Biol Chem 269:24550–24552PubMedPubMedCentralGoogle Scholar
  14. Chalancon G, Madan Babu M (2011) Structure and evolution of transcriptional regulatory networks. In: Storz G, Hengee R (eds) Bacterial stress responses, 2nd edn. ASM Press, Washington, DC, pp 3–16CrossRefGoogle Scholar
  15. Coux O, Tanaka K, Goldberg AL (1996) Structure and functions of the 20S and 26S proteasomes. Annu Rev Biochem 65:801–847PubMedCrossRefPubMedCentralGoogle Scholar
  16. de Jong WW, Leunissen JA, Voorter CE (1993) Evolution of the alpha-crystallin/small heat-shock protein family. Mol Biol Evol 10:103–126PubMedPubMedCentralGoogle Scholar
  17. Delauney A, Pflieger D, Barrault M, Vinh J, Toledano MB (2002) A thiol peroxidase ss an H2O2 receptor and redox-transducer in gene activation. Cell 111:471–481CrossRefGoogle Scholar
  18. Delic M, Rebnegger C, Wanka F et al (2012) Oxidative protein folding and unfolded protein response elicit differing redox regulation in endoplasmic reticulum and cytosol of yeast. Free Radic Biol Med 52:2000–2012PubMedCrossRefPubMedCentralGoogle Scholar
  19. Ferrer-Sueta G, Manta B, Botti H, Radi R, Trujillo M, Denicola A (2011) Factors affecting protein thiol reactivity and specificity in peroxide reduction. Chem Res Toxicol 24:434–450PubMedCrossRefPubMedCentralGoogle Scholar
  20. Frand AR, Kaiser CA (1998) The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell 1:161–170PubMedCrossRefPubMedCentralGoogle Scholar
  21. Freedman RB, Hirst TR, Tuite MF (1994) Protein disulphide isomerase: building bridges in protein folding. Trends Biochem Sci 19:331–336PubMedCrossRefPubMedCentralGoogle Scholar
  22. Gardner BM, Walter P (2011) Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response. Science 333:1891–1894PubMedPubMedCentralCrossRefGoogle Scholar
  23. Gillece P, Luz JM, Lennarz WJ, de La Cruz FJ, Römisch K (1999) Export of a cysteine-free misfolded secretory protein from the endoplasmic reticulum for degradation requires interaction with protein disulfide isomerase. J Cell Biol 147:1443–1456PubMedPubMedCentralCrossRefGoogle Scholar
  24. Givol D, Goldberger RF, Anfinsen CB (1964) Oxidation and disulfide interchange in the reactivation of reduced ribonuclease. J Biol Chem 239:3114–3116Google Scholar
  25. Graf PCF, Martinez-Yamout M, VanHaerents S, Lilie H, Dyson HJ, Jakob U (2004) Activation of the redox-regulated chaperone Hsp33 by domain unfolding. J Biol Chem 279:20529–20538PubMedCrossRefPubMedCentralGoogle Scholar
  26. Graumann J, Lilie H, Tang X et al (2001) Activation of the redox-regulated molecular chaperone Hsp33 – a two-step mechanism. Structure 9:377–387PubMedCrossRefPubMedCentralGoogle Scholar
  27. Groll M, Ditzel L, Lowe J, Stock D, Bochtler M, Bartunik HD, Huber R (1997) Structure of 20S proteasome from yeast at 2.4A resolution. Nature 386:463–471PubMedCrossRefPubMedCentralGoogle Scholar
  28. Grunwald MS, Pires AS, Zanotto-Filho A, Gasparotto J, Gelain DP, Demartini DR, Schöler CM, de Bittencourt PIH, Moreira JCF, Moreira JCF (2014) The oxidation of HSP70 is associated with functional impairment and lack of stimulatory capacity. Cell Stress Chaperones 19:913–925PubMedPubMedCentralCrossRefGoogle Scholar
  29. Hageman J, van Waarde MAWH, Zylicz A, Walerych D, Kampinga HH (2011) The diverse members of the mammalian HSP70 machine show distinct chaperone-like activities. Biochem J 435:127–142PubMedCrossRefPubMedCentralGoogle Scholar
  30. Hahn J, Hu Z, Thiele DJ, Iyer VR (2004) Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol 24:5249–5256PubMedPubMedCentralCrossRefGoogle Scholar
  31. Harding HP, Zhang Y, Zeng H et al (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11:619–633PubMedCrossRefPubMedCentralGoogle Scholar
  32. Harshman KD, Moye-Rowley WS, Parker CS (1988) Transcriptional activation by the SV40 AP-1 recognition element in yeast is mediated by a factor similar to AP-1 that is distinct from GCN4. Cell 53:321–330PubMedCrossRefPubMedCentralGoogle Scholar
  33. Haynes CM, Titus EA, Cooper AA (2004) Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. Mol Cell 15:767–776PubMedCrossRefPubMedCentralGoogle Scholar
  34. Haze K, Yoshida H, Yanagi H, Yura T, Mori K (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 10:3787–3799PubMedPubMedCentralCrossRefGoogle Scholar
  35. Helmann JD (2011) Regulation by alternative sigma factors. In: Storz G, Hengee R (eds) Bacterial stress responses, 2nd edn. ASM Press, Washington, DC, pp 31–43CrossRefGoogle Scholar
  36. Hetz C, Martinon F, Rodriguez D, Glimcher LH (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1219–1243CrossRefGoogle Scholar
  37. Hipp MS, Park SH, Hartl FU (2014) Proteostasis impairment in protein-misfolding and -aggregation diseases. Trends Cell Biol 24:506–514PubMedCrossRefPubMedCentralGoogle Scholar
  38. Hoffmann JH, Linke K, Graf PCF, Lilie H, Jakob U (2004) Identification of a redox-regulated chaperone network. EMBO J 23:160–168PubMedCrossRefPubMedCentralGoogle Scholar
  39. Hughes KT, Mathee, Kalai (1998) The anti-sigma factors. Annu Rev Microbiol 52:231–286PubMedCrossRefPubMedCentralGoogle Scholar
  40. Hyslop PA, Hinshawz DB, Halsey WA et al (1988) Mechanisms of oxidant-mediated cell injury. J Biol Chem 263:1665–1675PubMedPubMedCentralGoogle Scholar
  41. Jacobson T, Navarrete C, Sharma SK et al (2012) Arsenite interferes with protein folding and triggers formation of protein aggregates in yeast. J Cell Sci 125:5073–5083PubMedCrossRefPubMedCentralGoogle Scholar
  42. Jacobson T, Priya S, Sharma SK et al (2017) Cadmium causes misfolding and aggregation of cytosolic proteins in yeast. Mol Cell Biol 37:e00490–e00416PubMedPubMedCentralCrossRefGoogle Scholar
  43. Jahngen-Hodge J, Obin MS, Gong X et al (1997) Regulation of ubiquitin-conjugating enzymes by glutathione following oxidative stress. J Biol Chem 272:28218–28226PubMedCrossRefGoogle Scholar
  44. Jakob U, Gaestel M, Engel K, Buchner J (1993) Small heat shock proteins are molecular chaperones. J Biol Chem 268:1517–1520PubMedPubMedCentralGoogle Scholar
  45. Jakob U, Muse W, Eser M, Bardwell JCA (1999) Chaperone activity with a redox switch. Cell 96:341–352PubMedCrossRefPubMedCentralGoogle Scholar
  46. Jang HH, Lee KO, Chi YH et al (2004) Two enzymes in one: two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117:625–635PubMedCrossRefPubMedCentralGoogle Scholar
  47. Kästle M, Reeg S, Rogowska-Wrzesinska A, Grune T (2012) Chaperones, but not oxidized proteins, are ubiquitinated after oxidative stress. Free Radic Biol Med 53:1468–1477PubMedCrossRefPubMedCentralGoogle Scholar
  48. Kelner MJ, Alexander NM (1985) Methylene blue directly oxidizes glutathione without the intermediate formation of hydrogen peroxide. J Biol Chem 260:15168–15171PubMedPubMedCentralGoogle Scholar
  49. Klappa P, Freedman RB, Zimmermann R (1995) Protein disulphide isomerase and a lumenal cyclophilin-type peptidyl prolyl cis-trans isomerase are in transient contact with secretory proteins during late stages of translocation. Eur J Biochem 232:755–764PubMedCrossRefPubMedCentralGoogle Scholar
  50. Knittler MR, Haas IG (1992) Interaction of BiP with newly synthesized immunoglobulin light chain molecules: cycles of sequential binding and release. EMBO J 11:1573–1581PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kortemme T, Creighton TE (1995) Ionisation of cysteine residues at the termini of model alpha-helical peptides. Relevance to unusual thiol pKa values in proteins of the thioredoxin family. J Mol Biol 253:799–812PubMedCrossRefPubMedCentralGoogle Scholar
  52. Kuge S, Jones N (1994) YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides. EMBO J 13:655–664PubMedPubMedCentralCrossRefGoogle Scholar
  53. Kuge S, Toda T, Iizuka N, Nomoto A (1998) Crm1 (XpoI) dependent nuclear export of the budding yeast transcription factor yAP-1 is sensitive to oxidative stress. Genes Cells 3:521–532PubMedCrossRefPubMedCentralGoogle Scholar
  54. Laboissiere MC, Sturley SL, Raines RT (1995) The essential function of protein-disulphide isomerase is to unscramble non-native disulphide bonds. J Biol Chem 270:28006–28009PubMedCrossRefPubMedCentralGoogle Scholar
  55. Le Moan N, Clement G, Le Maout S, Tacnet F, Toledano MB (2006) The Saccharomyces cerevisiae proteome of oxidized protein thiols: contrasted functions for the thioredoxin and glutathione pathways. J Biol Chem 281:10420–10430PubMedCrossRefPubMedCentralGoogle Scholar
  56. Lee S-J, Kim SJ, Kim I-K et al (2003) Crystal structures of human DJ-1 and Escherichia coli Hsp31, which share an evolutionarily conserved domain. J Biol Chem 278:44552–44559PubMedCrossRefPubMedCentralGoogle Scholar
  57. Liu XD, Thiele DJ (1996) Oxidative stress induced heat shock factor phosphorylation and HSF-dependent activation of yeast metallothionein gene transcription. Genes Dev 10:592–603PubMedCrossRefPubMedCentralGoogle Scholar
  58. Malki A, Kern R, Abdallah J, Richarme G (2003) Characterization of the Escherichia coli YedU protein as a molecular chaperone. Biochem Biophys Res Commun 301:430–436PubMedCrossRefPubMedCentralGoogle Scholar
  59. Marino SM, Gladyshev VN (2010) Cysteine function governs its conservation and degeneration and restricts its utilization on protein surfaces. J Mol Biol 404:902–916PubMedPubMedCentralCrossRefGoogle Scholar
  60. Marnett LJ, Riggins JN, West JD (2003) Endogenous generation of reactive oxidants and electrophiles and their reactions with DNA and protein. J Clin Invest 111:583–593PubMedPubMedCentralCrossRefGoogle Scholar
  61. Martinat C, Shendelman S, Jonason A et al (2004) Sensitivity to oxidative stress in DJ-1-deficient dopamine neurons: an ES-derived cell model of primary Parkinsonism. PLoS Biol 2:e327PubMedPubMedCentralCrossRefGoogle Scholar
  62. Merksamer PI, Trusina A, Papa FR (2008) Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions. Cell 135:933–947PubMedPubMedCentralCrossRefGoogle Scholar
  63. Meunier L, Usherwood Y-K, Chung KT, Hendershot LM (2002) A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol Biol Cell 13:4456–4469PubMedPubMedCentralCrossRefGoogle Scholar
  64. Miyata Y, Rauch JN, Jinwal UK, Thompson AD, Srinivasan S, Dickey CA, Gestwicki JE (2012) Cysteine reactivity distinguishes redox sensing by the heat-inducible and constitutive forms of heat shock protein 70. Chem Biol 19:1391–1399PubMedPubMedCentralCrossRefGoogle Scholar
  65. Molteni SN, Fassio A, Ciriolo MR, Filomeni G, Pasqualetto E, Fagioli C, Sitia R (2004) Glutathione limits Ero1-dependent oxidation in the endoplasmic reticulum. J Biol Chem 279:32667–32673PubMedCrossRefPubMedCentralGoogle Scholar
  66. Morano KA, Grant CM, Moye-Rowley WS (2012) The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics 190:1157–1195PubMedPubMedCentralCrossRefGoogle Scholar
  67. Mori K, Ogawa N, Kawahara T, Yanagi H, Yura T (2000) mRNA splicing-mediated C-terminal replacement of transcription factor Hac1p is required for efficient activation of the unfolded protein response. Proc Natl Acad Sci U S A 97:4660–4665PubMedPubMedCentralCrossRefGoogle Scholar
  68. Mujacic M, Baneyx F (2006) Regulation of Escherichia coli hchA, a stress-inducible gene encoding molecular chaperone Hsp31. Mol Microbiol 60:1576–1589PubMedCrossRefPubMedCentralGoogle Scholar
  69. Mujacic M, Bader MW, Baneyx F (2004) Escherichia coli Hsp31 functions as a holding chaperone that cooperates with the DnaK-DnaJ-GrpE system in the management of protein misfolding under severe stress conditions. Mol Microbiol 51:849–859PubMedCrossRefPubMedCentralGoogle Scholar
  70. Nardai G, Stadler K, Papp E, Korcsmáros T, Jakus J, Csermely P (2005) Diabetic changes in the redox status of the microsomal protein folding machinery. Biochem Biophys Res Commun 334:787–795PubMedCrossRefPubMedCentralGoogle Scholar
  71. Ng DT, Watowich SS, Lamb RA (1992) Analysis in vivo of GRP78-BiP/substrate interactions and their role in induction of the GRP78-BiP gene. Mol Biol Cell 3:143–155PubMedPubMedCentralCrossRefGoogle Scholar
  72. Noiva R, Freedman RB, Lennarz WJ (1993) Peptide binding to protein disulfide isomerase occurs at a site distinct from the active sites. J Biol Chem 268:19210–19217PubMedPubMedCentralGoogle Scholar
  73. Pajares M, Jiménez-Moreno N, Dias IHK et al (2015) Redox control of protein degradation. Redox Biol 6:409–420PubMedPubMedCentralCrossRefGoogle Scholar
  74. Paulsen CE, Carroll KS (2010) Orchestrating redox signaling networks through regulatory cysteine switches. ACS Chem Biol 5:47–62PubMedPubMedCentralCrossRefGoogle Scholar
  75. Petrucelli L, Dickson D, Kehoe K et al (2004) CHIP and Hsp70 regulate tau ubiquitination, degradation and aggregation. Hum Mol Genet 13:703–714PubMedCrossRefPubMedCentralGoogle Scholar
  76. Poole LB (2015) The basics of thiols and cysteines in redox biology and chemistry. Free Radic Biol Med 80:148–157PubMedCrossRefPubMedCentralGoogle Scholar
  77. Quigley PM, Korotkov K, Baneyx F, Hol WGJ (2004) A new native EcHsp31 structure suggests a key role of structural flexibility for chaperone function. Protein Sci 13:269–277PubMedPubMedCentralCrossRefGoogle Scholar
  78. Reinheckel T, Sitte N, Ullrich O, Kuckelkorn U, Davies KJ, Grune T (1998) Comparative resistance of the 20S and 26S proteasome to oxidative stress. Biochem J 335:637–642PubMedPubMedCentralCrossRefGoogle Scholar
  79. Richmond CS, Glasner JD, Mau R, Jin H, Blattner FR (1999) Genome-wide expression profiling in Escherichia coli K-12. Nucleic Acids Res 27:3821–3835PubMedPubMedCentralCrossRefGoogle Scholar
  80. Röhl A, Rohrberg J, Buchner J (2013) The chaperone Hsp90: changing partners for demanding clients. Trends Biochem Sci 38:253–262PubMedCrossRefPubMedCentralGoogle Scholar
  81. Rüegsegger U, Leber JH, Walter P (2001) Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 107:103–114PubMedCrossRefPubMedCentralGoogle Scholar
  82. Sánchez-Gómez FJ, Díez-Dacal B, Pajares M, Llorca O, Pérez-Sala D (2010) Cyclopentenone prostaglandins with dienone structure promote cross-linking of the chemoresistance-inducing enzyme glutathione transferase P1-1. Mol Pharmacol 78:723–733PubMedCrossRefPubMedCentralGoogle Scholar
  83. Sastry MSR, Quigley PM, Hol WGJ, Baneyx F (2004) The linker-loop region of Escherichia coli chaperone Hsp31 functions as a gate that modulates high-affinity substrate binding at elevated temperatures. Proc Natl Acad Sci U S A 101:8587–8592PubMedPubMedCentralCrossRefGoogle Scholar
  84. Schröder E, Ponting CP (1998) Evidence that peroxiredoxins are novel members of the thioredoxin fold superfamily. Protein Sci 7:2465–2468PubMedPubMedCentralCrossRefGoogle Scholar
  85. Sharma SK, Goloubinoff P, Christen P (2008) Heavy metal ions are potent inhibitors of protein folding. Biochem Biophys Res Commun 372:341–345PubMedCrossRefPubMedCentralGoogle Scholar
  86. Shen SC, Yang LY, Lin HY, Wu CY, Su TH, Chen YC (2008) Reactive oxygen species-dependent HSP90 protein cleavage participates in arsenical As+ 3- and MMA+ 3-induced apoptosis through inhibition of telomerase activity via JNK activation. Toxicol Appl Pharmacol 229:239–251PubMedCrossRefPubMedCentralGoogle Scholar
  87. Shendelman S, Jonason A, Martinat C, Leete T, Abeliovich A (2004) DJ-1 is a redox-dependent molecular chaperone that inhibits alpha-synuclein aggregate formation. PLoS Biol 2:e362PubMedPubMedCentralCrossRefGoogle Scholar
  88. Siegenthaler KD, Pareja KA, Wang J, Sevier CS (2017) An unexpected role for the yeast nucleotide exchange factor Sil1 as a reductant acting on the molecular chaperone BiP. Elife 6:e24141PubMedPubMedCentralCrossRefGoogle Scholar
  89. Silva GM, Netto LES, Simões V et al (2012) Redox control of 20S proteasome gating. Antioxid Redox Signal 16:1183–1194PubMedPubMedCentralCrossRefGoogle Scholar
  90. Skoneczna A, Miciałkiewicz A, Skoneczny M (2007) Saccharomyces cerevisiae Hsp31p, a stress response protein conferring protection against reactive oxygen species. Free Radic Biol Med 42:1409–1420PubMedCrossRefPubMedCentralGoogle Scholar
  91. Solís EJ, Pandey JP, Zheng X et al (2016) Defining the essential function of yeast Hsf1 reveals a compact transcriptional program for maintaining eukaryotic proteostasis. Mol Cell 63:60–71PubMedPubMedCentralCrossRefGoogle Scholar
  92. Subedi KP, Choi D, Kim I, Min B, Park C (2011) Hsp31 of Escherichia coli K-12 is glyoxalase III. Mol Microbiol 81:926–936PubMedCrossRefPubMedCentralGoogle Scholar
  93. Sugiyama K, Izawa S, Inoue Y (2000) The Yap1p-dependent induction of glutathione synthesis in heat shock response of Saccharomyces cerevisiae. J Biol Chem 275:15535–15540PubMedCrossRefPubMedCentralGoogle Scholar
  94. Szabo A, Langer T, Schroder H, Flanagan J, Bukau B, Hartl FU (1994) The ATP hydrolysis-dependent reaction cycle of the Escherichia coli Hsp70 system DnaK, DnaJ, and GrpE. Proc Natl Acad Sci U S A 91:10345–10349PubMedPubMedCentralCrossRefGoogle Scholar
  95. Tamás MJ, Sharma SK, Ibstedt S, Jacobson T, Christen P (2014) Heavy metals and metalloids as a cause for protein misfolding and aggregation. Biomol Ther 4:252–267Google Scholar
  96. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101:249–258PubMedCrossRefPubMedCentralGoogle Scholar
  97. Trott A, West JD, Klaić L, Westerheide SD, Silverman RB, Morimoto RI, Morano KA (2008) Activation of heat shock and antioxidant responses by the natural product celastrol: transcriptional signatures of a thiol-targeted molecule. Mol Biol Cell 19:1104–1112PubMedPubMedCentralCrossRefGoogle Scholar
  98. Tsai CJ, Aslam K, Drendel HM et al (2015) Hsp31 is a stress response chaperone that intervenes in the protein misfolding process. J Biol Chem 290:24816–24834PubMedPubMedCentralCrossRefGoogle Scholar
  99. Tu BP, Weissman JS (2004) Oxidative protein folding in eukaryotes: mechanisms and consequences. J Cell Biol 164:341–346PubMedPubMedCentralCrossRefGoogle Scholar
  100. Tu BP, Ho-Schleyer SC, Travers KJ, Weissman JS (2000) Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 290:1571–1574PubMedCrossRefPubMedCentralGoogle Scholar
  101. Valastyan JS, Lindquist S (2014) Mechanisms of protein-folding diseases at a glance. Dis Model Mech 7:9–14PubMedPubMedCentralCrossRefGoogle Scholar
  102. Veal EA, Ross SJ, Malakasi P, Peacock E, Morgan BA (2003) Ybp1 is required for the hydrogen peroxide-induced oxidation of the Yap1 transcription factor. J Biol Chem 278:30896–30904PubMedCrossRefPubMedCentralGoogle Scholar
  103. Verghese J, Abrams J, Wang Y, Morano KA (2012) Biology of the heat shock response and protein chaperones: budding yeast (Saccharomyces cerevisiae) as a model system. Microbiol Mol Biol Rev 76:115–158PubMedPubMedCentralCrossRefGoogle Scholar
  104. Wallace EWJ, Kear-Scott JL, Pilipenko EV et al (2015) Reversible, specific, active aggregates of endogenous proteins assemble upon heat stress. Cell 162:1286–1298PubMedPubMedCentralCrossRefGoogle Scholar
  105. Wang J, Sevier CS (2016) Formation and reversibility of BiP protein cysteine oxidation facilitate cell survival during and post oxidative stress. J Biol Chem 291:7541–7557PubMedPubMedCentralCrossRefGoogle Scholar
  106. Wang CC, Tsou CL (1993) Protein disulfide isomerase is both an enzyme and a chaperone. FASEB J 7:1515–1517PubMedCrossRefPubMedCentralGoogle Scholar
  107. Wang AM, Morishima Y, Clapp KM et al (2010) Inhibition of Hsp70 by methylene blue affects signaling protein function and ubiquitination and modulates polyglutamine protein degradation. J Biol Chem 285:15714–15723PubMedPubMedCentralCrossRefGoogle Scholar
  108. Wang Y, Gibney PA, West JD, Morano KA (2012) The yeast Hsp70 Ssa1 is a sensor for activation of the heat shock response by thiol-reactive compounds. Mol Biol Cell 23:3290–3298PubMedPubMedCentralCrossRefGoogle Scholar
  109. Wang J, Pareja KA, Kaiser CA, Sevier CS (2014) Redox signaling via the molecular chaperone BiP protects cells against endoplasmic reticulum-derived oxidative stress. elife 3:e03496PubMedPubMedCentralCrossRefGoogle Scholar
  110. Wei J, Hendershot LM (1995) Characterization of the nucleotide binding properties and ATPase activity of recombinant hamster BiP purified from bacteria. J Biol Chem 270:26670–26676PubMedCrossRefPubMedCentralGoogle Scholar
  111. Weids AJ, Grant CM (2014) The yeast peroxiredoxin Tsa1 protects against protein-aggregate-induced oxidative stress. J Cell Sci 127:1327–1335PubMedPubMedCentralCrossRefGoogle Scholar
  112. Weids AJ, Ibstedt S, Tamás MJ, Grant CM (2016) Distinct stress conditions result in aggregation of proteins with similar properties. Sci Rep 6:1–12CrossRefGoogle Scholar
  113. West JD, Stamm CE, Brown HA, Justice SL, Morano KA (2011) Enhanced toxicity of the protein cross-linkers divinyl sulfone and diethyl acetylenedicarboxylate in comparison to related monofunctional electrophiles. Chem Res Toxicol 24:1457–1459PubMedCrossRefPubMedCentralGoogle Scholar
  114. West JD, Wang Y, Morano KA (2012) Small molecule activators of the heat shock response: chemical properties, molecular targets, and therapeutic promise. Chem Res Toxicol 25:2036–2053PubMedPubMedCentralCrossRefGoogle Scholar
  115. Wilson MA, St Amour CV, Collins JL, Ringe D, Petsko GA (2004) The 1.8-A resolution crystal structure of YDR533Cp from Saccharomyces cerevisiae: a member of the DJ-1/ThiJ/PfpI superfamily. Proc Natl Acad Sci U S A 101:1531–1536PubMedPubMedCentralCrossRefGoogle Scholar
  116. Winter J, Linke K, Jatzek A, Jakob U (2005) Severe oxidative stress causes inactivation of DnaK and activation of the redox-regulated chaperone Hsp33. Mol Cell 17:381–392PubMedCrossRefPubMedCentralGoogle Scholar
  117. Winterbourn CC, Hampton MB (2008) Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45:549–561PubMedCrossRefPubMedCentralGoogle Scholar
  118. Wood MJ, Storz G, Tjandra N (2004) Structural basis for redox regulation of Yap1 transcription factor localization. Nature 430:917–921PubMedCrossRefPubMedCentralGoogle Scholar
  119. Xu M, Marsh HM, Sevier CS (2016) A conserved cysteine within the ATPase domain of the endoplasmic reticulum chaperone BiP is necessary for a complete complement of BiP activities. J Mol Biol 428:4168–4184PubMedPubMedCentralCrossRefGoogle Scholar
  120. Yan C, Lee LH, Davis LI (1998) Crm1p mediates regulated nuclear export of a yeast AP-1-like transcription factor. EMBO J 17:7416–7429PubMedPubMedCentralCrossRefGoogle Scholar
  121. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881–891PubMedCrossRefPubMedCentralGoogle Scholar
  122. Zhang YS, Kolm RH, Mannervik B, Talalay P (1995) Reversible conjugation of isothiocyanates with glutathione catalyzed by human glutathione transferases. Biochem Biophys Res Commun 206:748–755PubMedCrossRefPubMedCentralGoogle Scholar
  123. Zhang H, Yang J, Wu S, Gong W, Chen C, Perrett S (2016) Glutathionylation of the bacterial Hsp70 chaperone DnaK provides a link between oxidative stress and the heat shock response. J Biol Chem 291:6967–6981PubMedCrossRefPubMedCentralGoogle Scholar
  124. Zheng X, Krakowiak J, Patel N, Beyzavi A, Ezike J, Khalil AS, Pincus D (2016) Dynamic control of Hsf1 during heat shock by a chaperone switch and phosphorylation. elife 5:e18638PubMedPubMedCentralCrossRefGoogle Scholar
  125. Zhou Y, Gottesman S, Hoskins JR, Maurizi MR, Wickner S (2001) The RssB response regulator directly targets σS for degradation by ClpXP. Genes Dev 15:627–637PubMedPubMedCentralCrossRefGoogle Scholar
  126. Zhou W, Zhu M, Wilson MA, Petsko GA, Fink AL (2006) The oxidation state of DJ-1 regulates its chaperone activity toward alpha-synuclein. J Mol Biol 356:1036–1048PubMedCrossRefPubMedCentralGoogle Scholar
  127. Zmijewski JW, Banerjee S, Abraham E (2009) S-glutathionylation of the Rpn2 regulatory subunit inhibits 26 S proteasomal function. J Biol Chem 284:22213–22221PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Microbiology and Molecular GeneticsUniversity of Texas McGovern Medical School at HoustonHoustonUSA
  2. 2.MD Anderson UT Health Graduate School of Biomedical SciencesHoustonUSA

Personalised recommendations