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Review Article

ClpB/Hsp100 proteins and heat stress tolerance in plants

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Pages 862-874 | Received 22 Apr 2014, Accepted 29 Apr 2015, Published online: 30 Jun 2015

References

  • Agarwal M, Sahi C, Katiyar-Agarwal S, et al. (2003). Molecular characterization of rice hsp101: complementation of yeast hsp104 mutation by disaggregation of protein granules and differential expression in indica and japonica rice types. Plant Mol Biol, 51, 543–53
  • Allan E, Mullany P, Tabaqchali S. (1998). Construction and characterization of a Helicobacter pylori clpB mutant and role of the gene in the stress response. J Bacteriol, 180, 426–9
  • Barnett ME, Zolkiewski M. (2002). Site-directed mutagenesis of conserved charged amino acid residues in ClpB from Escherichia coli. Biochemistry, 41, 11277–83
  • Barnett ME, Zolkiewska A, Zolkiewski M. (2000). Structure and activity of ClpB from Escherichia coli. Role of the amino-and -carboxyl-terminal domains. J Biol Chem, 275, 37565–71
  • Bita CE, Gerats T. (2013). Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci, 4, 273
  • Bosl B, Grimminger V, Walter S. (2005). Substrate binding to the molecular chaperone Hsp104 and its regulation by nucleotides. J Biol Chem, 280, 38170–6
  • Butler SM, Festa RA, Pearce MJ, et al. (2006). Self-compartmentalized bacterial proteases and pathogenesis. Mol Microbiol, 60, 553–62
  • Campbell JL, Klueva NY, Zheng HG, et al. (2001). Cloning of new members of heat shock protein HSP101 gene family in wheat (Triticum aestivum (L.) Moench) inducible by heat, dehydration, and ABA(1). Biochim Biophys Acta, 1517, 270–7
  • Carr T, Wang Y, Huang Z, et al. (2006). Tobamovirus infection is independent of HSP101 mRNA induction and protein expression. Virus Res, 121, 33–41
  • Cashikar AG, Schirmer EC, Hattendorf DA, et al. (2002). Defining a pathway of communication from the C-terminal peptide binding domain to the N-terminal ATPase domain in a AAA protein. Mol Cell, 9, 751–60
  • Chang CC, Huang PS, Lin HR, et al. (2007). Transactivation of protein expression by rice HSP101 in planta and using Hsp101 as a selection marker for transformation. Plant Cell Physiol, 48, 1098–107
  • Desantis ME, Shorter J. (2012). The elusive middle domain of Hsp104 and ClpB: location and function. Biochim Biophys Acta, 1823, 29–39
  • Dinkova TD, Zepeda H, Martinez-Salas E, et al. (2005). Cap-independent translation of maize Hsp101. Plant J, 41, 722–31
  • Dougan DA, Mogk A, Bukau B. (2002). Protein folding and degradation in bacteria: to degrade or not to degrade? That is the question. Cell Mol Life Sci, 59, 1607–16
  • Dougan DA, Weber-Ban E, Bukau B. (2003). Targeted delivery of an ssrA-tagged substrate by the adaptor protein SspB to its cognate AAA+ protein ClpX. Mol Cell, 12, 373–80
  • Doyle SM, Shorter J, Zolkiewski M, et al. (2007). Asymmetric deceleration of ClpB or Hsp104 ATPase activity unleashes protein-remodeling activity. Nat Struct Mol Biol, 14, 114–22
  • Eriksson MJ, Clarke AK. (2000). The Escherichia coli heat shock protein ClpB restores acquired thermotolerance to a cyanobacterial clpB deletion mutant. Cell Stress Chaperones, 5, 255–64
  • Ferreira PC, Ness F, Edwards SR, et al. (2001). The elimination of the yeast [PSI+] prion by guanidine hydrochloride is the result of Hsp104 inactivation. Mol Microbiol, 40, 1357–69
  • Glover JR, Lindquist S. (1998). Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell, 94, 73–82
  • Goloubinoff P, Mogk A, Zvi AP, et al. (1999). Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci USA, 96, 13732–7
  • Gottesman S, Clark WP, Maurizi MR. (1990). The ATP-dependent Clp protease of Escherichia coli. Sequence of clpA and identification of a Clp-specific substrate. J Biol Chem, 265, 7886–93
  • Gottesman S. (2003). Proteolysis in bacterial regulatory circuits. Annu Rev Cell Dev Biol, 19, 565–87
  • Gould SB, Waller RF, McFadden GI. (2008). Plastid evolution. Annu Rev Plant Biol, 59, 491–517
  • Grover A, Mittal D, Negi M, et al. (2013). Generating high temperature tolerant transgenic plants: achievements and challenges. Plant Sci, 205–206, 38–47
  • Hattendorf DA, Lindquist SL. (2002). Cooperative kinetics of both Hsp104 ATPase domains and interdomain communication revealed by AAA sensor-1 mutants. EMBO J, 21, 12–21
  • Hillier LD, Lennon G, Becker M, et al. (1996). Generation and analysis of 280,000 human expressed sequence tags. Genome Res, 6, 807–28
  • Hong SW, Vierling E. (2000). Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci USA, 97, 4392–7
  • Hong SW, Vierling E. (2001). Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. Plant J, 27, 25–35
  • Hwang BJ, Park WJ, Chung CH, et al. (1987). Escherichia coli contains a soluble ATP-dependent protease (Ti) distinct from protease La. Proc Natl Acad Sci USA, 84, 5550–4
  • Jung G, Jones G, Masison DC. (2002). Amino acid residue 184 of yeast Hsp104 chaperone is critical for prion-curing by guanidine, prion propagation, and thermotolerance. Proc Natl Acad Sci USA, 99, 9936–41
  • Katayama-Fujimura Y, Gottesman S, Maurizi MR. (1987). A multiple-component, ATP-dependent protease from Escherichia coli. J Biol Chem, 262, 4477–85
  • Katiyar-Agarwal S, Agarwal M, Grover A. (2003). Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant Mol Biol, 51, 677–86
  • Kedzierska S, Akoev V, Barnett ME, et al. (2003). Structure and function of the middle domain of ClpB from Escherichia coli. Biochemistry, 42, 14242–8
  • Keeler SJ, Boettger CM, Haynes JG, et al. (2000). Acquired thermotolerance and expression of the HSP100/ClpB genes of lima bean. Plant Physiol, 123, 1121–32
  • Kim M, Lee U, Small I, et al. (2012). Mutations in an Arabidopsis mitochondrial transcription termination factor-related protein enhance thermotolerance in the absence of the major molecular chaperone HSP101. Plant Cell, 24, 3349–65
  • Konieczny I, Liberek K. (2002). Cooperative action of Escherichia coli ClpB protein and DnaK chaperone in the activation of a replication initiation protein. J Biol Chem, 277, 18483–8
  • Krzewska J, Langer T, Liberek K. (2001). Mitochondrial Hsp78, a member of the Clp/Hsp100 family in Saccharomyces cerevisiae, cooperates with Hsp70 in protein refolding. FEBS Lett, 489, 92–6
  • Kurahashi H, Nakamura Y. (2007). Channel mutations in Hsp104 hexamer distinctively affect thermotolerance and prion-specific propagation. Mol Microbiol, 63, 1669–83
  • Lazaro-Mixteco PE, Nieto-Sotelo J, Swatek KN, et al. (2012). The absence of heat shock protein HSP101 affects the proteome of mature and germinating maize embryos. J Proteome Res, 11, 3246–58
  • Lee YR, Nagao RT, Key JL. (1994). A soybean 101-kD heat shock protein complements a yeast HSP104 deletion mutant in acquiring thermotolerance. Plant Cell, 6, 1889–97
  • Lee U, Wie C, Escobar M, et al. (2005). Genetic analysis reveals domain interactions of Arabidopsis Hsp100/ClpB and cooperation with the small heat shock protein chaperone system. Plant Cell, 17, 559–71
  • Lee U, Rioflorido I, Hong SW, et al. (2006). The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. Plant J, 49, 115–27
  • Li J, Sha B. (2003). Crystal structure of the E. coli Hsp100 ClpB N-terminal domain. Structure, 11, 323–8
  • Lin MY, Chai KH, Ko SS, et al. (2014). A positive feedback loop between HEAT SHOCK PROTEIN101 and HEAT STRESS-ASSOCIATED 32-KD PROTEIN modulates long-term acquired thermotolerance illustrating diverse heat stress responses in rice varieties. Plant Physiol, 164, 2045–53
  • Ling J, Wells DR, Tanguay RL, et al. (2000). Heat shock protein HSP101 binds to the Fed-1 internal light regulator y element and mediates its high translational activity. Plant Cell, 12, 1213–27
  • Lipinska N, Zietkiewicz S, Sobczak A, et al. (2013). Disruption of ionic interactions between the nucleotide binding domain 1 (NBD1) and middle (M) domain in Hsp100 disaggregase unleashes toxic hyperactivity and partial independence from Hsp70. J Biol Chem, 288, 2857–69
  • Liu Z, Tek V, Akoev V, et al. (2002). Conserved amino acid residues within the amino-terminal domain of ClpB are essential for the chaperone activity. J Mol Biol, 321, 111–20
  • Lum R, Tkach JM, Vierling E, et al. (2004). Evidence for an unfolding/threading mechanism for protein disaggregation by Saccharomyces cerevisiae Hsp104. J Biol Chem, 279, 29139–46
  • Mackay RG, Helsen CW, Tkach JM, et al. (2008). The C-terminal extension of Saccharomyces cerevisiae Hsp104 plays a role in oligomer assembly. Biochemistry, 47, 1918–27
  • Miot M, Reidy M, Doyle SM, et al. (2011). Species-specific collaboration of heat shock proteins (Hsp) 70 and 100 in thermotolerance and protein disaggregation. Proc Natl Acad Sci USA, 108, 6915–20
  • Mishra RC, Grover A. (2014). Intergenic sequence between Arabidopsis caseinolytic protease B-cytoplasmic/heat shock protein100 and choline kinase genes functions as a heat-inducible bidirectional promoter. Plant Physiol, 166, 1646–58
  • Mizuno S, Nakazaki Y, Yoshida M, et al. (2012). Orientation of the amino-terminal domain of ClpB affects the disaggregation of the protein. FEBS J, 279, 1474–84
  • Mogk A, Tomoyasu T, Goloubinoff P, et al. (1999). Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J, 1999, 18, 6934–49
  • Mogk A, Schlieker C, Strub C, et al. (2003). Roles of individual domains and conserved motifs of the AAA+ chaperone ClpB in oligomerization, ATP hydrolysis, and chaperone activity. J Biol Chem, 278, 17615–24
  • Mogk A, Haslberger T, Tessarz P, et al. (2008). Common and specific mechanisms of AAA+ proteins involved in protein quality control. Biochem Soc Trans, 36, 120–5
  • Motohashi K, Watanabe Y, Yohda M, et al. (1999). Heat-inactivated proteins are rescued by the DnaK.J-GrpE set and ClpB chaperones. Proc Natl Acad Sci USA, 96, 7184–9
  • Myouga F, Motohashi R, Kuromori T, et al. (2006). An Arabidopsis chloroplast-targeted Hsp101 homologue, APG6, has an essential role in chloroplast development as well as heat-stress response. Plant J, 48, 249–60
  • Nieto-Sotelo J, Kannan KB, Martinez LM, et al. (1999). Characterization of a maize heat-shock protein 101 gene, HSP101, encoding a ClpB/Hsp100 protein homologue. Gene, 230, 187–95
  • Nieto-Sotelo J, Martinez LM, Ponce G, et al. (2002). Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth. Plant Cell, 14, 1621–33
  • Oguchi Y, Kummer E, Seyffer F, et al. (2012). A tightly regulated molecular toggle controls AAA+ disaggregase. Nat Struct Mol Biol, 19, 1338–46
  • Parsell DA, Sanchez Y, Stitzel JD, et al. (1991). Hsp104 is a highly conserved protein with two essential nucleotide-binding sites. Nature, 353, 270–3
  • Parsell DA, Kowal AS, Singer MA, et al. (1994). Protein disaggregation mediated by heat-shock protein Hsp104. Nature, 372, 475–8
  • Pontis E, Sun XY, Jornvall H, et al. (1991). ClpB proteins copurify with the anaerobic Escherichia coli reductase. Biochem Biophys Res Commun, 180, 1222–6
  • Porankiewicz J, Clarke AK. (1997). Induction of the heat shock protein ClpB affects cold acclimation in the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol, 179, 5111–17
  • Queitsch C, Hong SW, Vierling E, et al. (2000). Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell, 12, 479–92
  • Reidy M, Miot M, Masison DC. (2012). Prokaryotic chaperones support yeast prions and thermotolerance and define disaggregation machinery interactions. Genetics, 192, 185–93
  • Sanchez Y, Lindquist SL. (1990). HSP104 required for induced thermotolerance. Science, 248, 1112–15
  • Sanchez Y, Taulien J, Borkovich KA, et al. (1992). Hsp104 is required for tolerance to many forms of stress. EMBO J, 11, 2357–64
  • Schaupp A, Marcinowski M, Grimminger V, et al. (2007). Processing of proteins by the molecular chaperone Hsp104. J Mol Biol, 370, 674–86
  • Schelin J, Lindmark F, Clarke AK. (2002). The clpP multigene family for the ATP-dependent Clp protease in the cyanobacterium Synechococcus. Microbiology, 148, 2255–65
  • Schirmer EC, Lindquist S, Vierling E. (1994). An Arabidopsis heat shock protein complements a thermotolerance defect in yeast. Plant Cell, 6, 1899–909
  • Schirmer EC, Queitsch C, Kowal AS, et al. (1998). The ATPase activity of Hsp104, effects of environmental conditions and mutations. J Biol Chem, 273, 15546–52
  • Schirmer EC, Ware DM, Queitsch C, et al. (2001). Subunit interactions influence the biochemical and biological properties of Hsp104. Proc Natl Acad Sci USA, 98, 914–19
  • Schirmer EC, Homann OR, Kowal AS, et al. (2004). Dominant gain-of-function mutations in Hsp104p reveal crucial roles for the middle region. Mol Biol Cell, 15, 2061–72
  • Schlieker C, Weibezahn J, Patzelt H, et al. (2004). Substrate recognition by the AAA+ chaperone ClpB. Nat Struct Mol Biol, 11, 607–15
  • Schlieker C, Zentgraf H, Dersch P, et al. (2005). ClpV, a unique Hsp100/Clp member of pathogenic proteobacteria. Biol Chem, 386, 1115–27
  • Shanklin J, DeWitt ND, Flanagan JM. (1995). The stroma of higher plant plastids contain ClpP and ClpC, functional homologs of Escherichia coli ClpP and ClpA: an archetypal two-component ATP-dependent protease. Plant Cell, 7, 1713–22
  • Sielaff B, Tsai FT. (2010). The M-domain controls Hsp104 protein remodeling activity in an Hsp70/Hsp40-dependent manner. J Mol Biol, 402, 30–7
  • Singh A, Grover A. (2010). Plant Hsp100/ClpB-like proteins: poorly-analyzed cousins of yeast ClpB machine. Plant Mol Biol, 74, 395–404
  • Singh A, Singh U, Mittal D, et al. (2010). Genome-wide analysis of rice ClpB/HSP100, ClpC and ClpD genes. BMC Genomics, 11, 95
  • Singh A, Mittal D, Lavania D, et al. (2012). OsHsfA2c and OsHsfB4b are involved in the transcriptional regulation of cytoplasmic OsClpB (Hsp100) gene in rice (Oryza sativa L.). Cell Stress Chaperones, 17, 243–54
  • Singla SL, Grover A. (1993). Antibodies raised against yeast HSP 104 cross-react with a heat- and abscisic acid-regulated polypeptide in rice. Plant Mol Biol, 22, 1177–80
  • Singla SL, Pareek A, Kush AK, et al. (1998). Distribution patterns of 104 kDa stress-associated protein in rice. Plant Mol Biol, 37, 911–19
  • Squires CL, Pedersen S, Ross BM, et al. (1991). ClpB is the Escherichia coli heat shock protein F84.1. J Bacteriol, 173, 4254–62
  • Tessarz P, Mogk A, Bukau B. (2008). Substrate threading through the central pore of the Hsp104 chaperone as a common mechanism for protein disaggregation and prion propagation. Mol Microbiol, 68, 87–97
  • Tkach JM, Glover JR. (2008). Nucleocytoplasmic trafficking of the molecular chaperone Hsp104 in unstressed and heat-shocked cells. Traffic, 9, 39–56
  • Tonsor SJ, Scott C, Boumaza I, et al. (2008). Heat shock protein 101 effects in A. thaliana: genetic variation, fitness and pleiotropy in controlled temperature conditions. Mol Ecol, 17, 1614–26
  • Wang KH, Sauer RT, Baker TA. (2007). ClpS modulates but is not essential for bacterial N-end rule degradation. Genes Dev, 21, 403–8
  • Watanabe YH, Motohashi K, Taguchi H, et al. (2000). Heat-inactivated proteins managed by DnaKJ-GrpE-ClpB chaperones are released as a chaperonin-recognizable non-native form. J Biol Chem, 275, 12388–92
  • Watanabe YH, Motohashi K, Yoshida M. (2002). Roles of the two ATP binding sites of ClpB from Thermus thermophilus. J Biol Chem, 277, 5804–9
  • Weibezahn J, Tessarz P, Schlieker C, et al. (2004). Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell, 119, 653–65
  • Wells DR, Tanguay RL, Le H, et al. (1998). HSP101 functions as a specific translational regulatory protein whose activity is regulated by nutrient status. Genes Dev, 12, 3236–51
  • Wendler P, Shorter J, Plisson C, et al. (2007). Atypical AAA+ subunit packing creates an expanded cavity for disaggregation by the protein-remodeling factor Hsp104. Cell, 131, 1366–77
  • Yang JY, Sun Y, Sun AQ, et al. (2006). The involvement of chloroplast HSP100/ClpB in the acquired thermotolerance in tomato. Plant Mol Biol, 62, 385–95
  • Young TE, Ling J, Geisler-Lee CJ, et al. (2001). Developmental and thermal regulation of the maize heat shock protein, HSP101. Plant Physiol, 127, 777–91
  • Zhang T, Ploetz EA, Nagy M, et al. (2012). Flexible connection of the N-terminal domain in ClpB modulates substrate binding and the aggregate reactivation efficiency. Proteins, 80, 2758–68
  • Zolkiewski M. (2006). A camel passes through the eye of a needle: protein unfolding activity of Clp ATPases. Mol Microbiol, 61, 1094–100
  • Zybailov B, Friso G, Kim J, et al. (2009). Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism. Mol Cell Proteomics, 8, 1789–810

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