GrpE, Hsp110/Grp170, HspBP1/Sil1 and BAG Domain Proteins: Nucleotide Exchange Factors for Hsp70 Molecular Chaperones
- ️Wed Jan 01 2014
Abrams JL, Verghese J, Gibney PA, Morano KA (2014) Hierarchical functional specificity of cytosolic heat shock protein 70 (Hsp70) nucleotide exchange factors in yeast J Biol Chem 289:13155–13167
Ahner A, Whyte FM, Brodsky JL (2005) Distinct but overlapping functions of Hsp70, Hsp90, and an Hsp70 nucleotide exchange factor during protein biogenesis in yeast. Arch Biochem Biophys 435:32–41
Alberti S, Esser C, Höhfeld J (2003) BAG-1- a nucleotide exchange factor of Hsc70 with multiple cellular functions. Cell Stress Chaperones 8:225–231
Alberti S, Bohse K, Arndt V, Schmitz A, Höhfeld J (2004) The co-chaperone HspBP1 inhibits the CHIP ubiquitin ligase and stimulates the maturation of the cystic fibrosis transmembrane conductance regulator. Mol Biol Cell 15:4003–4010
Andreasson C, Fiaux J, Rampelt H, Mayer MP, Bukau B (2008) Hsp110 is a nucleotide-activated exchange factor for Hsp70. J Biol Chem 283:8877–8884
Andreasson C, Rampelt H, Fiaux J, Druffel-Augustin S, Bukau B (2010) The endoplasmic reticulum Grp170 acts as a nucleotide exchange factor of Hsp70 via a mechanism similar to that of the cytosolic Hsp110. J Biol Chem 285:12445–12453
Ang D, Georgopoulos C (1989) The heat-shock-regulated grpE gene of Escherichia coli is required for bacterial growth at all temperatures but is dispensable in certain mutant backgrounds. J Bacteriol 171:2748–2755
Antoku K, Maser RS, Scully WJ Jr, Delach SM, Johnson DE (2001) Isolation of Bcl-2 binding proteins that exhibit homology with BAG-1 and suppressor of death domains protein. Biochem Biophys Res Commun 286:1003–1010
Anttonen AK, Mahjneh I, Hamalainen RH, Lagier-Tourenne C, Kopra O, Waris L, Anttonen M, Joensuu T, Kalimo H, Paetau A, Tranebjaerg L, Chaigne D, Koenig M, Eeg-Olofsson O, Udd B, Somer M, Somer H, Lehesjoki AE (2005) The gene disrupted in Marinesco-Sjogren syndrome encodes SIL1, an HSPA5 cochaperone. Nat Genet 37:1309–1311
Arakawa A, Handa N, Ohsawa N, Shida M, Kigawa T, Hayashi F, Shirouzu M, Yokoyama S (2010) The C-terminal BAG domain of BAG5 induces conformational changes of the Hsp70 nucleotide-binding domain for ADP-ATP exchange. Structure 18:309–319
Arakawa A, Handa N, Shirouzu M, Yokoyama S (2011) Biochemical and structural studies on the high affinity of Hsp70 for ADP. Protein Sci 20:1367–1379
Arndt V, Daniel C, Nastainczyk W, Alberti S, Höhfeld J (2005) BAG-2 acts as an inhibitor of the chaperone-associated ubiquitin ligase CHIP. Mol Biol Cell 16:5891–5900
Arndt V, Dick N, Tawo R, Dreiseidler M, Wenzel D, Hesse M, Fürst DO, Saftig P, Saint R, Fleischmann BK, Hoch M, Höhfeld J (2010) Chaperone-assisted selective autophagy is essential for muscle maintenance. Curr Biol 20:143–148
Balch WE, Morimoto RI, Dillin A, Kelly JW (2008) Adapting proteostasis for disease intervention. Science 319:916–919
Bertelsen EB, Chang L, Gestwicki JE, Zuiderweg ER (2009) Solution conformation of wild-type E. coli Hsp70 (DnaK) chaperone complexed with ADP and substrate. Proc Natl Acad Sci U S A 106:8471–8476
Bimston D, Song J, Winchester D, Takayama S, Reed JC, Morimoto RI (1998) BAG-1, a negative regulator of Hsp70 chaperone activity, uncouples nucleotide hydrolysis from substrate release. EMBO J 17:6871–6878
Binici J, Koch J (2013) BAG-6, a jack of all trades in health and disease. Cell Mol Life Sci. doi:10.1007/s00018–013-1522-y
Brehmer D, Rüdiger S, Gässler CS, Klostermeier D, Packschies L, Reinstein J, Mayer MP, Bukau B (2001) Tuning of chaperone activity of Hsp70 proteins by modulation of nucleotide exchange. Nat Struct Biol 8:427–432
Briknarova K, Takayama S, Brive L, Havert ML, Knee DA, Velasco J, Homma S, Cabezas E, Stuart J, Hoyt DW, Satterthwait AC, Llinas M, Reed JC, Ely KR (2001) Structural analysis of BAG1 cochaperone and its interactions with Hsc70 heat shock protein. Nat Struct Biol 8:349–352
Briknarova K, Takayama S, Homma S, Baker K, Cabezas E, Hoyt DW, Li Z, Satterthwait AC, Ely KR (2002) BAG4/SODD protein contains a short BAG domain. J Biol Chem 277:31172–31178
Brockmann C, Leitner D, Labudde D, Diehl A, Sievert V, Büssow K, Kühne R, Oschkinat H (2004) The solution structure of the SODD BAG domain reveals additional electrostatic interactions in the HSP70 complexes of SODD subfamily BAG domains. FEBS Lett 558:101–106
Brodsky JL, Bracher A (2007) Nucleotide Exchange Factors for Hsp70 Molecular Chaperones. In: Balch GL (ed) Networking of chaperones by co-chaperones. Molecular Biology Intelligence Unit. Landes Biosciences, Austin, pp 1–12
Bukau B, Weissman J, Horwich A (2006) Molecular chaperones and protein quality control. Cell 125:443–451
Carrettiero DC, Hernandez I, Neveu P, Papagiannakopoulos T, Kosik KS (2009) The cochaperone BAG2 sweeps paired helical filament- insoluble tau from the microtubule. J Neurosci 29:2151–2161
Chang YW, Sun YJ, Wang C, Hsiao CD (2008) Crystal structures of the 70-kDa heat shock proteins in domain disjoining conformation. J Biol Chem 283:15502–15511
Chung KS, Hoe KL, Kim KW, Yoo HS (1998) Isolation of a novel heat shock protein 70-like gene, pss1 + of Schizosaccharomyces pombe homologous to hsp110/SSE subfamily. Gene 210:143–150
Chung KT, Shen Y, Hendershot LM (2002) BAP, a mammalian BiP-associated protein, is a nucleotide exchange factor that regulates the ATPase activity of BiP. J Biol Chem 277:47557–47563
Colinet H, Hoffmann A (2010) Gene and protein expression of Drosophila Starvin during cold stress and recovery from chill coma. Insect Biochem Mol Biol 40:425–428
Coulson M, Robert S, Saint R (2005) Drosophila starvin encodes a tissue-specific BAG-domain protein required for larval food uptake. Genetics 171:1799–1812
Dai Q, Qian SB, Li HH, McDonough H, Borchers C, Huang D, Takayama S, Younger JM, Ren HY, Cyr DM, Patterson C (2005) Regulation of the cytoplasmic quality control protein degradation pathway by BAG2. J Biol Chem 280:38673–38681
de Keyzer J, Steel GJ, Hale SJ, Humphries D, Stirling CJ (2009) Nucleotide binding by Lhs1p is essential for its nucleotide exchange activity and for function in vivo. J Biol Chem 284:31564–31571
Demand J, Alberti S, Patterson C, Höhfeld J (2001) Cooperation of a ubiquitin domain protein and an E3 ubiquitin ligase during chaperone/proteasome coupling. Curr Biol 11:1569–1577
Doong H, Price J, Kim YS, Gasbarre C, Probst J, Liotta LA, Blanchette J, Rizzo K, Kohn E (2000) CAIR-1/BAG-3 forms an EGF-regulated ternary complex with phospholipase C-gamma and Hsp70/Hsc70. Oncogene 19:4385–4395
Doong H, Vrailas A, Kohn EC (2002) What’s in the ‘BAG’?–A functional domain analysis of the BAG-family proteins. Cancer Lett 188:25–32
Dorard C, de Thonel A, Collura A, Marisa L, Svrcek M, Lagrange A, Jego G, Wanherdrick K, Joly AL, Buhard O, Gobbo J, Penard-Lacronique V, Zouali H, Tubacher E, Kirzin S, Selves J, Milano G, Etienne-Grimaldi MC, Bengrine-Lefevre L, Louvet C, Tournigand C, Lefevre JH, Parc Y, Tiret E, Flejou JF, Gaub MP, Garrido C, Duval A (2011) Expression of a mutant HSP110 sensitizes colorectal cancer cells to chemotherapy and improves disease prognosis. Nat Med 17:1283–1289
Doukhanina EV, Chen S, van der Zalm E, Godzik A, Reed J, Dickman MB (2006) Identification and functional characterization of the BAG protein family in Arabidopsis thaliana. J Biol Chem 281:18793–18801
Dragovic Z, Broadley SA, Shomura Y, Bracher A, Hartl FU (2006a) Molecular chaperones of the Hsp110 family act as nucleotide exchange factors of Hsp70s. EMBO J 25:2519–2528
Dragovic Z, Shomura Y, Tzvetkov N, Hartl FU, Bracher A (2006b) Fes1p acts as a nucleotide exchange factor for the ribosome-associated molecular chaperone Ssb1p. Biol Chem 387:1593–1600
Easton DP, Kaneko Y, Subjeck JR (2000) The hsp110 and Grp1 70 stress proteins: newly recognized relatives of the Hsp70s. Cell Stress Chaperones 5:276–290
Eroglu B, Moskophidis D, Mivechi NF (2010) Loss of Hsp110 leads to age-dependent tau hyperphosphorylation and early accumulation of insoluble amyloid beta. Mol Cell Biol 30:4626–4643
Fan Q, Park KW, Du Z, Morano KA, Li L (2007) The role of Sse1 in the de novo formation and variant determination of the [PSI+] prion. Genetics 177:1583–1593
Fang S, Li L, Cui B, Men S, Shen Y, Yang X (2013) Structural insight into plant programmed cell death mediated by BAG proteins in Arabidopsis thaliana. Acta Crystallogr D Biol Crystallogr 69:934–945
Flaherty KM, DeLuca-Flaherty C, McKay DB (1990) Three-dimensional structure of the ATPase fragment of a 70 K heat-shock cognate protein. Nature 346:623–628
Franceschelli S, Rosati A, Lerose R, De Nicola S, Turco MC, Pascale M (2008) Bag3 gene expression is regulated by heat shock factor 1. J Cell Physiol 215:575–577
Fuchs M, Poirier DJ, Seguin SJ, Lambert H, Carra S, Charette SJ, Landry J (2010) Identification of the key structural motifs involved in HspB8/HspB6-Bag3 interaction. Biochem J 425:245–255
Gamerdinger M, Hajieva P, Kaya AM, Wolfrum U, Hartl FU, Behl C (2009) Protein quality control during aging involves recruitment of the macroautophagy pathway by BAG3. EMBO J 28:889–901
Gässler CS, Wiederkehr T, Brehmer D, Bukau B, Mayer MP (2001) Bag-1M accelerates nucleotide release for human Hsc70 and Hsp70 and can act concentration-dependent as positive and negative cofactor. J Biol Chem 276:32538–32544
Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O’Shea EK, Weissman JS (2003) Global analysis of protein expression in yeast. Nature 425:737–741
Goeckeler JL, Stephens A, Lee P, Caplan AJ, Brodsky JL (2002) Overexpression of yeast Hsp110 homolog Sse1p suppresses ydj1–151 thermosensitivity and restores Hsp90-dependent activity. Mol Biol Cell 13:2760–2770
Goeckeler JL, Petruso AP, Aguirre J, Clement CC, Chiosis G, Brodsky JL (2008) The yeast Hsp110, Sse1p, exhibits high-affinity peptide binding. FEBS Lett 582:2393–2396
Gong Y, Kakihara Y, Krogan N, Greenblatt J, Emili A, Zhang Z, Houry WA (2009) An atlas of chaperone–protein interactions in Saccharomyces cerevisiae: implications to protein folding pathways in the cell. Mol Syst Biol 5:275
Gonzalez B, de Graaf A, Renaud M, Sahm H (2000) Dynamic in vivo (31)P nuclear magnetic resonance study of Saccharomyces cerevisiae in glucose-limited chemostat culture during the aerobic-anaerobic shift. Yeast 16:483–497
Gowda NK, Kandasamy G, Froehlich MS, Dohmen RJ, Andreasson C (2013) Hsp70 nucleotide exchange factor Fes1 is essential for ubiquitin-dependent degradation of misfolded cytosolic proteins. Proc Natl Acad Sci U S A 110:5975–5980
Gupta RS (1998) Protein phylogenies and signature sequences: A reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev 62:1435–1491
Hale SJ, Lovell SC, de Keyzer J, Stirling CJ (2010) Interactions between Kar2p and its nucleotide exchange factors Sil1p and Lhs1p are mechanistically distinct. J Biol Chem 285:21600–21606
Harrison CJ, Hayer-Hartl M, Di Liberto M, Hartl F, Kuriyan J (1997) Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 276:431–435
Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475:324–332
Held T, Barakat AZ, Mohamed BA, Paprotta I, Meinhardt A, Engel W, Adham IM (2011) Heat-shock protein HSPA4 is required for progression of spermatogenesis. Reproduction 142:133–144
Höhfeld J, Jentsch S (1997) GrpE-like regulation of the hsc70 chaperone by the anti-apoptotic protein BAG-1. EMBO J 16:6209–6216
Homma S, Iwasaki M, Shelton GD, Engvall E, Reed JC, Takayama S (2006) BAG3 deficiency results in fulminant myopathy and early lethality. Am J Pathol 169:761–773
Horst M, Oppliger W, Rospert S, Schönfeld HJ, Schatz G, Azem A (1997) Sequential action of two hsp70 complexes during protein import into mitochondria. EMBO J 16:1842–1849
Howes J, Shimizu Y, Feige MJ, Hendershot LM (2012) C-terminal mutations destabilize SIL1/BAP and can cause Marinesco-Sjogren syndrome. J Biol Chem 287:8552–8560
Hu C, Lin SY, Chi WT, Charng YY (2012) Recent gene duplication and subfunctionalization produced a mitochondrial GrpE, the nucleotide exchange factor of the Hsp70 complex, specialized in thermotolerance to chronic heat stress in Arabidopsis. Plant Physiol 158:747–758
Huang HW, Yu C (2013) The NMR solution structure of the ubiquitin homology domain of Bcl-2-associated athanogene 1 (BAG-1-UBH) from Mus musculus. Biochem Biophys Res Commun 431:86–91
Ikeda E, Yoshida S, Mitsuzawa H, Uno I, Toh-e A (1994) YGE1 is a yeast homologue of Escherichia coli grpE and is required for maintenance of mitochondrial functions. FEBS Lett 339:265–268
Ishihara K, Yamagishi N, Saito Y, Adachi H, Kobayashi Y, Sobue G, Ohtsuka K, Hatayama T (2003) Hsp105alpha suppresses the aggregation of truncated androgen receptor with expanded CAG repeats and cell toxicity. J Biol Chem 278:25143–25150
Iwasaki M, Tanaka R, Hishiya A, Homma S, Reed JC, Takayama S (2010) BAG3 directly associates with guanine nucleotide exchange factor of Rap1, PDZGEF2, and regulates cell adhesion. Biochem Biophys Res Commun 400:413–418
Jacobs AT, Marnett LJ (2009) HSF1-mediated BAG3 expression attenuates apoptosis in 4-hydroxynonenal-treated colon cancer cells via stabilization of anti-apoptotic Bcl-2 proteins. J Biol Chem 284:9176–9183
Jiang Y, Woronicz JD, Liu W, Goeddel DV (1999) Prevention of constitutive TNF receptor 1 signaling by silencer of death domains. Science 283:543–546
Jungkunz I, Link K, Vogel F, Voll LM, Sonnewald S, Sonnewald U (2011) AtHsp70–15-deficient Arabidopsis plants are characterized by reduced growth, a constitutive cytosolic protein response and enhanced resistance to TuMV. Plant J 66:983–995
Kabani M, Beckerich JM, Gaillardin C (2000) Sls1p stimulates Sec63p-mediated activation of Kar2p in a conformation-dependent manner in the yeast endoplasmic reticulum. Mol Cell Biol 20:6923–6934
Kabani M, Beckerich JM, Brodsky JL (2002a) Nucleotide exchange factor for the yeast Hsp70 molecular chaperone Ssa1p. Mol Cell Biol 22:4677–4689
Kabani M, McLellan C, Raynes DA, Guerriero V, Brodsky JL (2002b) HspBP1, a homologue of the yeast Fes1 and Sls1 proteins, is an Hsc70 nucleotide exchange factor. FEBS Lett 531:339–342
Kabbage M, Dickman MB (2008) The BAG proteins: a ubiquitous family of chaperone regulators. Cell Mol Life Sci 65:1390–1402
Kalia SK, Lee S, Smith PD, Liu L, Crocker SJ, Thorarinsdottir TE, Glover JR, Fon EA, Park DS, Lozano AM (2004) BAG5 inhibits parkin and enhances dopaminergic neuron degeneration. Neuron 44:931–945
Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11:579–592
Kanelakis KC, Murphy PJ, Galigniana MD, Morishima Y, Takayama S, Reed JC, Toft DO, Pratt WB (2000) hsp70 interacting protein Hip does not affect glucocorticoid receptor folding by the hsp90-based chaperone machinery except to oppose the effect of BAG-1. BioChemistry 39:14314–14321
Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Hartl FU (2013) Molecular chaperone functions in protein folding and proteostasis. Annu Rev Biochem 82:323–355
Kitao Y, Hashimoto K, Matsuyama T, Iso H, Tamatani T, Hori O, Stern DM, Kano M, Ozawa K, Ogawa S (2004) ORP150/HSP12A regulates Purkinje cell survival: a role for endoplasmic reticulum stress in cerebellar development. J Neurosci 24:1486–1496
Kityk R, Kopp J, Sinning I, Mayer MP (2012) Structure and dynamics of the ATP-bound open conformation of Hsp70 chaperones. Mol Cell 48:863–874
Knapp RT, Wong MJ, Kollmannsberger LK, Gassen NC, Kretzschmar A, Zschocke J, Hafner K, Young JC, Rein T (2014) Hsp70 cochaperones HspBP1 and BAG-1M differentially regulate steroid hormone receptor function. PLoS One 9:e85415
Kopito RR (2000) Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 10:524–530
Koplin A, Preissler S, Ilina Y, Koch M, Scior A, Erhardt M, Deuerling E (2010) A dual function for chaperones SSB-RAC and the NAC nascent polypeptide-associated complex on ribosomes. J Cell Biol 189:57–68
Kriegenburg F, Jakopec V, Poulsen EG, Nielsen SV, Roguev A, Krogan N, Gordon C, Fleig U, Hartmann-Petersen R (2014) A chaperone-assisted degradation pathway targets kinetochore proteins to ensure genome stability. PLoS Genet 10:e1004140
Kuo Y, Ren S, Lao U, Edgar BA, Wang T (2013) Suppression of polyglutamine protein toxicity by co-expression of a heat-shock protein 40 and a heat-shock protein 110. Cell Death Dis 4:e833
Kwon KR, Ahn JY, Kim MS, Jung JY, Lee JH, Oh IH (2010) Disruption of bis leads to the deterioration of the vascular niche for hematopoietic stem cells. Stem Cells 28:268–278
Laloraya S, Gambill BD, Craig EA (1994) A role for a eukaryotic GrpE-related protein, Mge1p, in protein translocation. Proc Natl Acad Sci U S A 91:6481–6485
Laloraya S, Dekker PJ, Voos W, Craig EA, Pfanner N (1995) Mitochondrial GrpE modulates the function of matrix Hsp70 in translocation and maturation of preproteins. Mol Cell Biol 15:7098–7105
Lamark T, Johansen T (2012) Aggrephagy: selective disposal of protein aggregates by macroautophagy. Int J Cell Biol. doi:10.1155/2012/736905
Laufen T, Mayer MP, Beisel C, Klostermeier D, Mogk A, Reinstein J, Bukau B (1999) Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones. Proc Natl Acad Sci U S A 96:5452–5457
Li Z, Hartl FU, Bracher A (2013) Structure and function of Hip, an attenuator of the Hsp70 chaperone cycle. Nat Struct Mol Biol 20:929–935
Lin J, Hutchinson L, Gaston SM, Raab G, Freeman MR (2001) BAG-1 is a novel cytoplasmic binding partner of the membrane form of heparin-binding EGF-like growth factor: a unique role for proHB-EGF in cell survival regulation. J Biol Chem 276:30127–30132
Liu Q, Hendrickson WA (2007) Insights into Hsp70 chaperone activity from a crystal structure of the yeast Hsp110 Sse1. Cell 131:106–120
Liu XD, Morano KA, Thiele DJ (1999) The yeast Hsp110 family member, Sse1, is an Hsp90 cochaperone. J Biol Chem 274:26654–26660
Liu Y, Gierasch LM, Bahar I (2010) Role of Hsp70 ATPase domain intrinsic dynamics and sequence evolution in enabling its functional interactions with NEFs. PLoS Comput Biol 6. doi:10.1371/journal.pcbi.1000931
Makhnevych T, Wong P, Pogoutse O, Vizeacoumar FJ, Greenblatt JF, Emili A, Houry WA (2012) Hsp110 is required for spindle length control. J Cell Biol 198:623–636
Mandal AK, Gibney PA, Nillegoda NB, Theodoraki MA, Caplan AJ, Morano KA (2010) Hsp110 chaperones control client fate determination in the hsp70-Hsp90 chaperone system. Mol Biol Cell 21:1439–1448
Marada A, Allu PK, Murari A, PullaReddy B, Tammineni P, Thiriveedi VR, Danduprolu J, Sepuri NB (2013) Mge1, a nucleotide exchange factor of Hsp70, acts as an oxidative sensor to regulate mitochondrial Hsp70 function. Mol Biol Cell 24:692–703
Mariappan M, Li X, Stefanovic S, Sharma A, Mateja A, Keenan RJ, Hegde RS (2010) A ribosome-associating factor chaperones tail-anchored membrane proteins. Nature 466:1120–1124
Masison DC, Kirkland PA, Sharma D (2009) Influence of Hsp70s and their regulators on yeast prion propagation. Prion 3:65–73
Mattoo RU, Sharma SK, Priya S, Finka A, Goloubinoff P (2013) Hsp110 is a bona fide chaperone using ATP to unfold stable misfolded polypeptides and reciprocally collaborate with Hsp70 to solubilize protein aggregates. J Biol Chem 288:21399–21411
Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684
McClellan AJ, Scott MD, Frydman J (2005) Folding and quality control of the VHL tumor suppressor proceed through distinct chaperone pathways. Cell 121:739–748
Meacham GC, Patterson C, Zhang W, Younger JM, Cyr DM (2001) The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat Cell Biol 3:100–105
Miao B, Davis JE, Craig EA (1997) Mge1 functions as a nucleotide release factor for Ssc1, a mitochondrial Hsp70 of Saccharomyces cerevisiae. J Mol Biol 265:541–552
Mohamed BA, Barakat AZ, Held T, Elkenani M, Muhlfeld C, Manner J, Adham IM (2014) Respiratory distress and early neonatal lethality in hspa4 l/hspa4 double-mutant mice. Am J Respir Cell Mol Biol 50:817–824
Mokranjac D, Bourenkov G, Hell K, Neupert W, Groll M (2006) Structure and function of Tim14 and Tim16, the J and J-like components of the mitochondrial protein import motor. EMBO J 25:4675–4685
Moro F, Muga A (2006) Thermal adaptation of the yeast mitochondrial Hsp70 system is regulated by the reversible unfolding of its nucleotide exchange factor. J Mol Biol 358:1367–1377
Mukai H, Kuno T, Tanaka H, Hirata D, Miyakawa T, Tanaka C (1993) Isolation and characterization of SSE1 and SSE2, new members of the yeast HSP70 multigene family. Gene 132:57–66
Muralidharan V, Oksman A, Pal P, Lindquist S, Goldberg DE (2012) Plasmodium falciparum heat shock protein 110 stabilizes the asparagine repeat-rich parasite proteome during malarial fevers. Nat Commun 3:1310
Nakamura J, Fujimoto M, Yasuda K, Takeda K, Akira S, Hatayama T, Takagi Y, Nozaki K, Hosokawa N, Nagata K (2008) Targeted disruption of Hsp110/105 gene protects against ischemic stress. Stroke 39:2853–2859
Nakamura A, Takumi K, Miki K (2010) Crystal structure of a thermophilic GrpE protein: insight into thermosensing function for the DnaK chaperone system. J Mol Biol 396:1000–1011
Nikolaidis N, Nei M (2004) Concerted and nonconcerted evolution of the Hsp70 gene superfamily in two sibling species of nematodes. Mol Biol Evol 21:498–505
Oh HJ, Chen X, Subjeck JR (1997) Hsp110 protects heat-denatured proteins and confers cellular thermoresistance. J Biol Chem 272:31636–31640
Oh HJ, Easton D, Murawski M, Kaneko Y, Subjeck JR (1999) The chaperoning activity of hsp110. Identification of functional domains by use of targeted deletions. J Biol Chem 274:15712–15718
Olzscha H, Schermann SM, Woerner AC, Pinkert S, Hecht MH, Tartaglia GG, Vendruscolo M, Hayer-Hartl M, Hartl FU, Vabulas RM (2011) Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 144:67–78
Page RC, Xu Z, Amick J, Nix JC, Misra S (2012) Crystallization and preliminary X-ray crystallographic analysis of the Bag2 amino-terminal domain from Mus musculus. Acta Crystallogr Sect F Struct Biol Cryst Commun 68:647–651
Plesofsky-Vig N, Brambl R (1998) Characterization of an 88-kDa heat shock protein of Neurospora crassa that interacts with Hsp30. J Biol Chem 273:11335–11341
Polier S, Dragovic Z, Hartl FU, Bracher A (2008) Structural basis for the cooperation of Hsp70 and Hsp110 chaperones in protein folding. Cell 133:1068–1079
Polier S, Hartl FU, Bracher A (2010) Interaction of the Hsp110 molecular chaperones from S. cerevisiae with substrate protein. J Mol Biol 401:696–707
Qi R, Sarbeng EB, Liu Q, Le KQ, Xu X, Xu H, Yang J, Wong JL, Vorvis C, Hendrickson WA, Zhou L, Liu Q (2013) Allosteric opening of the polypeptide-binding site when an Hsp70 binds ATP. Nat Struct Mol Biol 20:900–907
Rampelt H, Kirstein-Miles J, Nillegoda NB, Chi K, Scholz SR, Morimoto RI, Bukau B (2012) Metazoan Hsp70 machines use Hsp110 to power protein disaggregation. EMBO J 31:4221–4235
Rauch JN, Gestwicki JE (2014) Binding of human nucleotide exchange factors to heat shock protein 70 (Hsp70) generates functionally distinct complexes in vitro. J Biol Chem 289:1402–1414
Raviol H, Bukau B, Mayer MP (2006a) Human and yeast Hsp110 chaperones exhibit functional differences. FEBS Lett 580:168–174
Raviol H, Sadlish H, Rodriguez F, Mayer MP, Bukau B (2006b) Chaperone network in the yeast cytosol: Hsp110 is revealed as an Hsp70 nucleotide exchange factor. EMBO J 25:2510–2518
Raynes DA, Guerriero V (1998) Inhibition of Hsp70 ATPase activity and protein renaturation by a novel Hsp70-binding protein. J Biol Chem 273:32883–32888
Rosati A, Graziano V, De Laurenzi V, Pascale M, Turco MC (2011) BAG3: a multifaceted protein that regulates major cell pathways. Cell Death Dis 2:e141
Rüdiger S, Germeroth 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
Sadlish H, Rampelt H, Shorter J, Wegrzyn RD, Andreasson C, Lindquist S, Bukau B (2008) Hsp110 chaperones regulate prion formation and propagation in S. cerevisiae by two discrete activities. PLoS One 3:e1763
Saxena A, Banasavadi-Siddegowda YK, Fan Y, Bhattacharya S, Roy G, Giovannucci DR, Frizzell RA, Wang X (2012) Human heat shock protein 105/110 kDa (Hsp105/110) regulates biogenesis and quality control of misfolded cystic fibrosis transmembrane conductance regulator at multiple levels. J Biol Chem 287:19158–19170
Schmidt S, Strub A, Rottgers K, Zufall N, Voos W (2001) The two mitochondrial heat shock proteins 70, Ssc1 and Ssq1, compete for the cochaperone Mge1. J Mol Biol 313:13–26
Schneider HC, Westermann B, Neupert W, Brunner M (1996) The nucleotide exchange factor MGE exerts a key function in the ATP-dependent cycle of mt-Hsp70-Tim44 interaction driving mitochondrial protein import. EMBO J 15:5796–5803
Schuermann JP, Jiang J, Cuellar J, Llorca O, Wang L, Gimenez LE, Jin S, Taylor AB, Demeler B, Morano KA, Hart PJ, Valpuesta JM, Lafer EM, Sousa R (2008) Structure of the Hsp110:Hsc70 nucleotide exchange machine. Mol Cell 31:232–243
Senderek J, Krieger M, Stendel C, Bergmann C, Moser M, Breitbach-Faller N, Rudnik-Schoneborn S, Blaschek A, Wolf NI, Harting I, North K, Smith J, Muntoni F, Brockington M, Quijano-Roy S, Renault F, Herrmann R, Hendershot LM, Schroder JM, Lochmuller H, Topaloglu H, Voit T, Weis J, Ebinger F, Zerres K (2005) Mutations in SIL1 cause Marinesco-Sjogren syndrome, a cerebellar ataxia with cataract and myopathy. Nat Genet 37:1312–1314
Shaner L, Trott A, Goeckeler JL, Brodsky JL, Morano KA (2004) The function of the yeast molecular chaperone Sse1 is mechanistically distinct from the closely related hsp70 family. J Biol Chem 279:21992–22001
Shaner L, Wegele H, Buchner J, Morano KA (2005) The yeast HSP110 SSE1 functionally interacts with the HSP70 chaperones SSA and SSB. J Biol Chem 279:21992–22001
Shaner L, Sousa R, Morano KA (2006) Characterization of Hsp70 binding and nucleotide exchange by the yeast Hsp110 chaperone Sse1. BioChemistry 45:15075–15084
Shaner L, Gibney PA, Morano KA (2008) The Hsp110 protein chaperone Sse1 is required for yeast cell wall integrity and morphogenesis. Curr Genet 54:1–11
Shi LX, Theg SM (2010) A stromal heat shock protein 70 system functions in protein import into chloroplasts in the moss Physcomitrella patens. Plant Cell 22:205–220
Shomura Y, Dragovic Z, Chang HC, Tzvetkov N, Young JC, Brodsky JL, Guerriero V, Hartl FU, Bracher A (2005) Regulation of Hsp70 function by HspBP1: Structural analysis reveals an alternate mechanism for Hsp70 nucleotide exchange. Mol Cell 17:367–379
Shorter J (2011) The mammalian disaggregase machinery: Hsp110 synergizes with Hsp70 and Hsp40 to catalyze protein disaggregation and reactivation in a cell-free system. PLoS One 6:e26319
Sondermann H, Scheufler C, Schneider C, Höhfeld J, Hartl FU, Moarefi I (2001) Structure of a Bag/Hsc70 complex: convergent functional evolution of Hsp70 nucleotide exchange factors. Science 291:1553–1557
Sondermann H, Ho AK, Listenberger LL, Siegers K, Moarefi I, Wente SR, Hartl FU, Young JC (2002) Prediction of novel Bag-1 homologs based on structure/function analysis identifies Snl1p as an Hsp70 co-chaperone in Saccharomyces cerevisiae. J Biol Chem 277:33220–33227
Song J, Takeda M, Morimoto RI (2001) Bag1-Hsp70 mediates a physiological stress signalling pathway that regulates Raf-1/ERK and cell growth. Nat Cell Biol 3:276–282
Steel GJ, Fullerton DM, Tyson JR, Stirling CJ (2004) Coordinated activation of Hsp70 chaperones. Science 303:98–101
Storozhenko S, De Pauw P, Kushnir S, Van Montagu M, Inze D (1996) Identification of an Arabidopsis thaliana cDNA encoding a HSP70-related protein belonging to the HSP110/SSE1 subfamily. FEBS Lett 390:113–118
Swain JF, Dinler G, Sivendran R, Montgomery DL, Stotz M, Gierasch LM (2007) Hsp70 chaperone ligands control domain association via an allosteric mechanism mediated by the interdomain linker. Mol Cell 26:27–39
Symersky J, Zhang Y, Schormann N, Li S, Bunzel R, Pruett P, Luan CH, Luo M (2004) Structural genomics of Caenorhabditis elegans: structure of the BAG domain. Acta Crystallogr D Biol Crystallogr 60:1606–1610
Takayama S, Reed JC (2001) Molecular chaperone targeting and regulation by BAG family proteins. Nat Cell Biol 3:E237–E241
Takayama S, Krajewski S, Krajewska M, Kitada S, Zapata JM, Kochel K, Knee D, Scudiero D, Tudor G, Miller GJ, Miyashita T, Yamada M, Reed JC (1998) Expression and location of Hsp70/Hsc-binding anti-apoptotic protein BAG-1 and its variants in normal tissues and tumor cell lines. Cancer Res 58:3116–3131
Takayama S, Xie Z, Reed JC (1999) An evolutionarily conserved family of Hsp70/Hsc70 molecular chaperone regulators. J Biol Chem 274:781–786
Tewari R, Bailes E, Bunting KA, Coates JC (2010) Armadillo-repeat protein functions: questions for little creatures. Trends Cell Biol 20:470–481
Trott A, Shaner L, Morano KA (2005) The molecular chaperone Sse1 and the growth control protein kinase Sch9 collaborate to regulate protein kinase A activity in Saccharomyces cerevisiae. Genetics 170:1009–1021
Tyson JR, Stirling CJ (2000) LHS1 and SIL1 provide a lumenal function that is essential for protein translocation into the endoplasmic reticulum. EMBO J 19:6440–6452
Tzankov S, Wong MJ, Shi K, Nassif C, Young JC (2008) Functional divergence between co-chaperones of Hsc70. J Biol Chem 283:27100–27109
Ulbricht A, Eppler FJ, Tapia VE, van der Ven PF, Hampe N, Hersch N, Vakeel P, Stadel D, Haas A, Saftig P, Behrends C, Fürst DO, Volkmer R, Hoffmann B, Kolanus W, Höhfeld J (2013) Cellular mechanotransduction relies on tension-induced and chaperone-assisted autophagy. Curr Biol 23:430–435
Ung PM, Thompson AD, Chang L, Gestwicki JE, Carlson HA (2013) Identification of key hinge residues important for nucleotide-dependent allostery in E. coli Hsp70/DnaK. PLoS Comput Biol 9:e1003279
Velten M, Gomez-Vrielynck N, Chaffotte A, Ladjimi MM (2002) Domain structure of the HSC70 cochaperone, HIP. J Biol Chem 277:259–266
Verghese J, Morano KA (2012) A lysine-rich region within fungal BAG domain-containing proteins mediates a novel association with ribosomes. Eukaryot Cell 11:1003–1011
Vogel M, Mayer MP, Bukau B (2006) Allosteric regulation of Hsp70 chaperones involves a conserved interdomain linker. J Biol Chem 281:38705–38711
Wada S, Hamada M, Satoh N (2006) A genomewide analysis of genes for the heat shock protein 70 chaperone system in the ascidian Ciona intestinalis. Cell Stress Chaperones 11:23–33
Wang X, Venable J, LaPointe P, Hutt DM, Koulov AV, Coppinger J, Gurkan C, Kellner W, Matteson J, Plutner H, Riordan JR, Kelly JW, Yates JR 3rd, Balch WE (2006) Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell 127:803–815
Wang J, Farr GW, Zeiss CJ, Rodriguez-Gil DJ, Wilson JH, Furtak K, Rutkowski DT, Kaufman RJ, Ruse CI, Yates JR 3rd, Perrin S, Feany MB, Horwich AL (2009) Progressive aggregation despite chaperone associations of a mutant SOD1-YFP in transgenic mice that develop ALS. Proc Natl Acad Sci U S A 106:1392–1397
Wang Q, Liu Y, Soetandyo N, Baek K, Hegde R, Ye Y (2011) A ubiquitin ligase-associated chaperone holdase maintains polypeptides in soluble states for proteasome degradation. Mol Cell 42:758–770
Wang AM, Miyata Y, Klinedinst S, Peng HM, Chua JP, Komiyama T, Li X, Morishima Y, Merry DE, Pratt WB, Osawa Y, Collins CA, Gestwicki JE, Lieberman AP (2013) Activation of Hsp70 reduces neurotoxicity by promoting polyglutamine protein degradation. Nat Chem Biol 9:112–118
Wilbanks SM, McKay DB (1995) How potassium affects the activity of the molecular chaperone Hsc70. II. Potassium binds specifically in the ATPase active site. J Biol Chem 270:2251–2257
Williams B, Kabbage M, Britt R, Dickman MB (2010) AtBAG7, an Arabidopsis Bcl-2-associated athanogene, resides in the endoplasmic reticulum and is involved in the unfolded protein response. Proc Natl Acad Sci U S A 107:6088–6093
Willmund F, Muhlhaus T, Wojciechowska M, Schroda M (2007) The NH2-terminal domain of the chloroplast GrpE homolog CGE1 is required for dimerization and cochaperone function in vivo. J Biol Chem 282:11317–11328
Willmund F, del Alamo M, Pechmann S, Chen T, Albanese V, Dammer EB, Peng J, Frydman J (2013) The cotranslational function of ribosome-associated Hsp70 in eukaryotic protein homeostasis. Cell 152:196–209
Wu CC, Naveen V, Chien CH, Chang YW, Hsiao CD (2012) Crystal structure of DnaK protein complexed with nucleotide exchange factor GrpE in DnaK chaperone system: insight into intermolecular communication. J Biol Chem 287:21461–21470
Xu Z, Page RC, Gomes MM, Kohli E, Nix JC, Herr AB, Patterson C, Misra S (2008) Structural basis of nucleotide exchange and client binding by the Hsp70 cochaperone Bag2. Nat Struct Mol Biol 15:1309–1317
Xu X, Sarbeng EB, Vorvis C, Kumar DP, Zhou L, Liu Q (2012) Unique peptide substrate binding properties of 110-kDa heat-shock protein (Hsp110) determine its distinct chaperone activity. J Biol Chem 287:5661–5672
Xu Z, Graham K, Foote M, Liang F, Rizkallah R, Hurt M, Wang Y, Wu Y, Zhou Y (2013) 14-3-3 protein targets misfolded chaperone-associated proteins to aggresomes. J Cell Sci 126:4173–4186
Yam AY, Albanese V, Lin HT, Frydman J (2005) HSP110 cooperates with different cytosolic HSP70 systems in a pathway for de novo folding. J Biol Chem 280:41252–41261
Yamashita H, Kawamata J, Okawa K, Kanki R, Nakamizo T, Hatayama T, Yamanaka K, Takahashi R, Shimohama S (2007) Heat-shock protein 105 interacts with and suppresses aggregation of mutant Cu/Zn superoxide dismutase: clues to a possible strategy for treating ALS. J Neurochem 102:1497–1505
Yan M, Li J, Sha B (2011) Structural analysis of the Sil1-Bip complex reveals the mechanism for Sil1 to function as a nucleotide-exchange factor. Biochem J 438:447–455
Zahn M, Berthold N, Kieslich B, Knappe D, Hoffmann R, Sträter N (2013) Structural studies on the forward and reverse binding modes of peptides to the chaperone DnaK. J Mol Biol 425:2463–2479
Zhang JX, Wang C, Yang CY, Wang JY, Chen L, Bao XM, Zhao YX, Zhang H, Liu J (2010) The role of Arabidopsis AtFes1A in cytosolic Hsp70 stability and abiotic stress tolerance. Plant J 62:539–548
Zhu X, Zhao X, Burkholder WF, Gragerov A, Ogata CM, Gottesman ME, Hendrickson WA (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272:1606–1614
Zhuravleva A, Clerico EM, Gierasch LM (2012) An interdomain energetic tug-of-war creates the allosterically active state in Hsp70 molecular chaperones. Cell 151:1296–1307