1932

Abstract

Small heat shock proteins (sHsps) constitute a diverse chaperone family that shares the α-crystallin domain, which is flanked by variable, disordered N- and C-terminal extensions. sHsps act as the first line of cellular defense against protein unfolding stress. They form dynamic, large oligomers that represent inactive storage forms. Stress conditions cause a rapid increase in cellular sHsp levels and trigger conformational rearrangements, resulting in exposure of substrate-binding sites and sHsp activation. sHsps bind to early-unfolding intermediates of misfolding proteins in an ATP-independent manner and sequester them in sHsp/substrate complexes. Sequestration protects substrates from further uncontrolled aggregation and facilitates their refolding by ATP-dependent Hsp70-Hsp100 disaggregases. Some sHsps with particularly strong sequestrase activity, such as yeast Hsp42, are critical factors for forming large, microscopically visible deposition sites of misfolded proteins in vivo. These sites are organizing centers for triaging substrates to distinct quality control pathways, preferentially Hsp70-dependent refolding and selective autophagy.

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2019-09-08
2024-12-03
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Literature Cited

  1. 1. 
    Ahmad MF, Raman B, Ramakrishna T, Rao M 2008. Effect of phosphorylation on αB-crystallin: differences in stability, subunit exchange and chaperone activity of homo and mixed oligomers of αB-crystallin and its phosphorylation-mimicking mutant. J. Mol. Biol. 375:1040–51
    [Google Scholar]
  2. 2. 
    Aquilina JA, Benesch JL, Ding LL, Yaron O, Horwitz J, Robinson CV 2005. Subunit exchange of polydisperse proteins: mass spectrometry reveals consequences of αA-crystallin truncation. J. Biol. Chem. 280:14485–91
    [Google Scholar]
  3. 3. 
    Arrasate M, Mitra S, Schweitzer ES, Segal MR, Finkbeiner S 2004. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431:805–10
    [Google Scholar]
  4. 4. 
    Arrigo AP. 2013. Human small heat shock proteins: protein interactomes of homo- and hetero-oligomeric complexes: an update. FEBS Lett 587:1959–69
    [Google Scholar]
  5. 5. 
    Baldwin AJ, Walsh P, Hansen DF, Hilton GR, Benesch JL et al. 2012. Probing dynamic conformations of the high-molecular-weight αB-crystallin heat shock protein ensemble by NMR spectroscopy. J. Am. Chem. Soc. 134:15343–50
    [Google Scholar]
  6. 6. 
    Basha E, Friedrich KL, Vierling E 2006. The N-terminal arm of small heat shock proteins is important for both chaperone activity and substrate specificity. J. Biol. Chem. 281:39943–52
    [Google Scholar]
  7. 7. 
    Basha E, Jones C, Wysocki V, Vierling E 2010. Mechanistic differences between two conserved classes of small heat shock proteins found in the plant cytosol. J. Biol. Chem. 285:11489–97
    [Google Scholar]
  8. 8. 
    Basha E, Lee GJ, Breci LA, Hausrath AC, Buan NR et al. 2004. The identity of proteins associated with a small heat shock protein during heat stress in vivo indicates that these chaperones protect a wide range of cellular functions. J. Biol. Chem. 279:7566–75
    [Google Scholar]
  9. 9. 
    Basha E, O'Neill H, Vierling E 2012. Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions. Trends Biochem. Sci. 37:106–17
    [Google Scholar]
  10. 10. 
    Bepperling A, Alte F, Kriehuber T, Braun N, Weinkauf S et al. 2012. Alternative bacterial two-component small heat shock protein systems. PNAS 109:20407–12
    [Google Scholar]
  11. 11. 
    Bissonnette SA, Rivera-Rivera I, Sauer RT, Baker TA 2010. The IbpA and IbpB small heat-shock proteins are substrates of the AAA+ Lon protease. Mol. Microbiol. 75:1539–49
    [Google Scholar]
  12. 12. 
    Bukach OV, Seit-Nebi AS, Marston SB, Gusev NB 2004. Some properties of human small heat shock protein Hsp20 (HspB6). Eur. J. Biochem. 271:291–302
    [Google Scholar]
  13. 13. 
    Bumagina Z, Gurvits B, Artemova N, Muranov K, Kurganov B 2010. Paradoxical acceleration of dithiothreitol-induced aggregation of insulin in the presence of a chaperone. Int. J. Mol. Sci. 11:4556–79
    [Google Scholar]
  14. 14. 
    Cashikar AG, Duennwald M, Lindquist SL 2005. A chaperone pathway in protein disaggregation: Hsp26 alters the nature of protein aggregates to facilitate reactivation by Hsp104. J. Biol. Chem. 280:23869–75
    [Google Scholar]
  15. 15. 
    Chen B, Retzlaff M, Roos T, Frydman J 2011. Cellular strategies of protein quality control. Cold Spring Harb. Perspect. Biol. 3:a004374
    [Google Scholar]
  16. 16. 
    Cheng G, Basha E, Wysocki VH, Vierling E 2008. Insights into small heat shock protein and substrate structure during chaperone action derived from hydrogen/deuterium exchange and mass spectrometry. J. Biol. Chem. 283:26634–42
    [Google Scholar]
  17. 17. 
    Cheng IH, Scearce-Levie K, Legleiter J, Palop JJ, Gerstein H et al. 2007. Accelerating amyloid-β fibrillization reduces oligomer levels and functional deficits in Alzheimer disease mouse models. J. Biol. Chem. 282:23818–28
    [Google Scholar]
  18. 18. 
    Clark AR, Vree Egberts W, Kondrat FDL, Hilton GR, Ray NJ et al. 2018. Terminal regions confer plasticity to the tetrameric assembly of human HspB2 and HspB3. J. Mol. Biol. 430:3297–310
    [Google Scholar]
  19. 19. 
    Coelho M, Lade SJ, Alberti S, Gross T, Tolic IM 2014. Fusion of protein aggregates facilitates asymmetric damage segregation. PLOS Biol 12:e1001886
    [Google Scholar]
  20. 20. 
    Cohen E, Bieschke J, Perciavalle RM, Kelly JW, Dillin A 2006. Opposing activities protect against age-onset proteotoxicity. Science 313:1604–10
    [Google Scholar]
  21. 21. 
    Cohen E, Paulsson JF, Blinder P, Burstyn-Cohen T, Du D et al. 2009. Reduced IGF-1 signaling delays age-associated proteotoxicity in mice. Cell 139:1157–69
    [Google Scholar]
  22. 22. 
    Delbecq SP, Klevit RE. 2013. One size does not fit all: the oligomeric states of αB crystallin. FEBS Lett 587:1073–80
    [Google Scholar]
  23. 23. 
    Duennwald ML, Echeverria A, Shorter J 2012. Small heat shock proteins potentiate amyloid dissolution by protein disaggregases from yeast and humans. PLOS Biol 10:e1001346
    [Google Scholar]
  24. 24. 
    Ehrnsperger M, Gräber S, Gaestel M, Buchner J 1997. Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J 16:221–29
    [Google Scholar]
  25. 25. 
    Escusa-Toret S, Vonk WI, Frydman J 2013. Spatial sequestration of misfolded proteins by a dynamic chaperone pathway enhances cellular fitness during stress. Nat. Cell Biol. 15:1231–43
    [Google Scholar]
  26. 26. 
    Fleckenstein T, Kastenmuller A, Stein ML, Peters C, Daake M et al. 2015. The chaperone activity of the developmental small heat shock protein Sip1 is regulated by pH-dependent conformational changes. Mol. Cell 58:1067–78
    [Google Scholar]
  27. 27. 
    Franzmann TM, Menhorn P, Walter S, Buchner J 2008. Activation of the chaperone Hsp26 is controlled by the rearrangement of its thermosensor domain. Mol. Cell 29:207–16
    [Google Scholar]
  28. 28. 
    Franzmann TM, Wuhr M, Richter K, Walter S, Buchner J 2005. The activation mechanism of Hsp26 does not require dissociation of the oligomer. J. Mol. Biol. 350:1083–93
    [Google Scholar]
  29. 29. 
    Frees D, Gerth U, Ingmer H 2014. Clp chaperones and proteases are central in stress survival, virulence and antibiotic resistance of Staphylococcusaureus.. Int. J. Med. Microbiol 304:142–49
    [Google Scholar]
  30. 30. 
    Freilich R, Arhar T, Abrams JL, Gestwicki JE 2018. Protein-protein interactions in the molecular chaperone network. Acc. Chem. Res. 51:940–49
    [Google Scholar]
  31. 31. 
    Friedrich KL, Giese KC, Buan NR, Vierling E 2004. Interactions between small heat shock protein subunits and substrate in small heat shock protein-substrate complexes. J. Biol. Chem. 279:1080–89
    [Google Scholar]
  32. 32. 
    Fu X, Shi X, Yan L, Zhang H, Chang Z 2013. In vivo substrate diversity and preference of small heat shock protein IbpB as revealed by using a genetically incorporated photo-cross-linker. J. Biol. Chem. 288:31646–54
    [Google Scholar]
  33. 33. 
    Fu X, Shi X, Yin L, Liu J, Joo K et al. 2013. Small heat shock protein IbpB acts as a robust chaperone in living cells by hierarchically activating its multi-type substrate-binding residues. J. Biol. Chem. 288:11897–906
    [Google Scholar]
  34. 34. 
    Fu X, Zhang H, Zhang X, Cao Y, Jiao W et al. 2005. A dual role for the N-terminal region of Mycobacterium tuberculosis Hsp16.3 in self-oligomerization and binding denaturing substrate proteins. J. Biol. Chem. 280:6337–48
    [Google Scholar]
  35. 35. 
    Garrido C, Paul C, Seigneuric R, Kampinga HH 2012. The small heat shock proteins family: the long forgotten chaperones. Int. J. Biochem. Cell Biol. 44:1588–92
    [Google Scholar]
  36. 36. 
    Gaubig LC, Waldminghaus T, Narberhaus F 2011. Multiple layers of control govern expression of the Escherichia coli ibpAB heat-shock operon. Microbiology 157:66–76
    [Google Scholar]
  37. 37. 
    Giese KC, Vierling E. 2002. Changes in oligomerization are essential for the chaperone activity of a small heat shock protein in vivo and in vitro. J. Biol. Chem. 277:46310–18
    [Google Scholar]
  38. 38. 
    Grousl T, Ungelenk S, Miller S, Ho CT, Khokhrina M et al. 2018. A prion-like domain in Hsp42 drives chaperone-facilitated aggregation of misfolded proteins. J. Cell Biol. 217:1269–85
    [Google Scholar]
  39. 39. 
    Guilbert SM, Lambert H, Rodrigue MA, Fuchs M, Landry J, Lavoie JN 2018. HSPB8 and BAG3 cooperate to promote spatial sequestration of ubiquitinated proteins and coordinate the cellular adaptive response to proteasome insufficiency. FASEB J 32:3518–35
    [Google Scholar]
  40. 40. 
    Hantke I, Schäfer H, Janczikowski A, Turgay K 2019. YocM a small heat shock protein can protect Bacillussubtilis cells during salt stress. Mol. Microbiol. 111:423–40
    [Google Scholar]
  41. 41. 
    Hartl FU, Bracher A, Hayer-Hartl M 2011. Molecular chaperones in protein folding and proteostasis. Nature 475:324–32
    [Google Scholar]
  42. 42. 
    Haslbeck M, Braun N, Stromer T, Richter B, Model N et al. 2004. Hsp42 is the general small heat shock protein in the cytosol of Saccharomycescerevisiae. EMBO J 23:638–49
    [Google Scholar]
  43. 43. 
    Haslbeck M, Franzmann T, Weinfurtner D, Buchner J 2005. Some like it hot: the structure and function of small heat-shock proteins. Nat. Struct. Mol. Biol. 12:842–46
    [Google Scholar]
  44. 44. 
    Haslbeck M, Ignatiou A, Saibil H, Helmich S, Frenzl E et al. 2004. A domain in the N-terminal part of Hsp26 is essential for chaperone function and oligomerization. J. Mol. Biol. 343:445–55
    [Google Scholar]
  45. 45. 
    Haslbeck M, Miess A, Stromer T, Walter S, Buchner J 2005. Disassembling protein aggregates in the yeast cytosol: the cooperation of Hsp26 with Ssa1 and Hsp104. J. Biol. Chem. 280:23861–68
    [Google Scholar]
  46. 46. 
    Haslbeck M, Vierling E. 2015. A first line of stress defense: small heat shock proteins and their function in protein homeostasis. J. Mol. Biol. 427:1537–48
    [Google Scholar]
  47. 47. 
    Haslbeck M, Walke S, Stromer T, Ehrnsperger M, White HE et al. 1999. Hsp26: a temperature-regulated chaperone. EMBO J 18:6744–51
    [Google Scholar]
  48. 48. 
    Haslbeck M, Weinkauf S, Buchner J 2019. Small heat shock proteins: Simplicity meets complexity. J. Biol. Chem. 294:2121–32
    [Google Scholar]
  49. 49. 
    Hochberg GKA, Ecroyd H, Liu C, Cox D, Cascio D et al. 2014. The structured core domain of αB-crystallin can prevent amyloid fibrillation and associated toxicity. PNAS 111:E1562–70
    [Google Scholar]
  50. 50. 
    Hochberg GKA, Shepherd DA, Marklund EG, Santhanagoplan I, Degiacomi MT et al. 2018. Structural principles that enable oligomeric small heat-shock protein paralogs to evolve distinct functions. Science 359:930–35
    [Google Scholar]
  51. 51. 
    Horwitz J. 1992. α-Crystallin can function as a molecular chaperone. PNAS 89:10449–53
    [Google Scholar]
  52. 52. 
    Hsu AL, Murphy CT, Kenyon C 2003. Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 300:1142–45
    [Google Scholar]
  53. 53. 
    Ito H, Kamei K, Iwamoto I, Inaguma Y, Nohara D, Kato K 2001. Phosphorylation-induced change of the oligomerization state of αB-crystallin. J. Biol. Chem. 276:5346–52
    [Google Scholar]
  54. 54. 
    Ito H, Okamoto K, Nakayama H, Isobe T, Kato K 1997. Phosphorylation of αB-crystallin in response to various types of stress. J. Biol. Chem. 272:29934–41
    [Google Scholar]
  55. 55. 
    Jakob U, Gaestel M, Engel K, Buchner J 1993. Small heat shock proteins are molecular chaperones. J. Biol. Chem. 268:1517–20
    [Google Scholar]
  56. 56. 
    Jaya N, Garcia V, Vierling E 2009. Substrate binding site flexibility of the small heat shock protein molecular chaperones. PNAS 106:15604–9
    [Google Scholar]
  57. 57. 
    Jiao W, Qian M, Li P, Zhao L, Chang Z 2005. The essential role of the flexible termini in the temperature-responsiveness of the oligomeric state and chaperone-like activity for the polydisperse small heat shock protein IbpB from Escherichia coli.J. Mol. Biol 347:871–84
    [Google Scholar]
  58. 58. 
    Kaganovich D, Kopito R, Frydman J 2008. Misfolded proteins partition between two distinct quality control compartments. Nature 454:1088–95
    [Google Scholar]
  59. 59. 
    Kampinga HH, Brunsting JF, Stege GJ, Konings AW, Landry J 1994. Cells overexpressing Hsp27 show accelerated recovery from heat-induced nuclear protein aggregation. Biochem. Biophys. Res. Commun. 204:1170–77
    [Google Scholar]
  60. 60. 
    Kato K, Ito H, Kamei K, Inaguma Y, Iwamoto I, Saga S 1998. Phosphorylation of αB-crystallin in mitotic cells and identification of enzymatic activities responsible for phosphorylation. J. Biol. Chem. 273:28346–54
    [Google Scholar]
  61. 61. 
    Kim KK, Kim R, Kim SH 1998. Crystal structure of a small heat-shock protein. Nature 394:595–99
    [Google Scholar]
  62. 62. 
    Kitagawa M, Matsumura Y, Tsuchido T 2000. Small heat shock proteins, IbpA and IbpB, are involved in resistances to heat and superoxide stresses in Escherichia coli.FEMSMicrobiol. Lett 184:165–71
    [Google Scholar]
  63. 63. 
    Kortmann J, Narberhaus F. 2012. Bacterial RNA thermometers: molecular zippers and switches. Nat. Rev. Microbiol. 10:255–65
    [Google Scholar]
  64. 64. 
    Krajewski SS, Joswig M, Nagel M, Narberhaus F 2014. A tricistronic heat shock operon is important for stress tolerance of Pseudomonasputida and conserved in many environmental bacteria. Environ. Microbiol. 16:1835–53
    [Google Scholar]
  65. 65. 
    Kriehuber T, Rattei T, Weinmaier T, Bepperling A, Haslbeck M, Buchner J 2010. Independent evolution of the core domain and its flanking sequences in small heat shock proteins. FASEB J 24:3633–42
    [Google Scholar]
  66. 66. 
    Laskowska E, Wawrzynow A, Taylor A 1996. IbpA and IbpB, the new heat-shock proteins, bind to endogenous Escherichia coli proteins aggregated intracellularly by heat shock. Biochimie 78:117–22
    [Google Scholar]
  67. 67. 
    Lee GJ, Roseman AM, Saibil HR, Vierling E 1997. A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J 16:659–71
    [Google Scholar]
  68. 68. 
    Lee S, Owen HA, Prochaska DJ, Barnum SR 2000. HSP16.6 is involved in the development of thermotolerance and thylakoid stability in the unicellular cyanobacterium, Synechocystis sp. PCC 6803. Curr. Microbiol. 40:283–87
    [Google Scholar]
  69. 69. 
    Lee U, Wie C, Escobar M, Williams B, Hong SW, Vierling E 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
    [Google Scholar]
  70. 70. 
    Lentze N, Aquilina JA, Lindbauer M, Robinson CV, Narberhaus F 2004. Temperature and concentration-controlled dynamics of rhizobial small heat shock proteins. Eur. J. Biochem. 271:2494–503
    [Google Scholar]
  71. 71. 
    Li Y, Xu X, Qu R, Zhang G, Rajoka MSR et al. 2018. Heterologous expression of Oenococcus oeni sHSP20 confers temperature stress tolerance in Escherichia coli. Cell Stress Chaperones 23:653–62
    [Google Scholar]
  72. 72. 
    Liu B, Larsson L, Caballero A, Hao X, Oling D et al. 2010. The polarisome is required for segregation and retrograde transport of protein aggregates. Cell 140:257–67
    [Google Scholar]
  73. 73. 
    Liu IC, Chiu SW, Lee HY, Leu JY 2012. The histone deacetylase Hos2 forms an Hsp42-dependent cytoplasmic granule in quiescent yeast cells. Mol. Biol. Cell 23:1231–42
    [Google Scholar]
  74. 74. 
    Liu Z, Wang C, Li Y, Zhao C, Li T et al. 2018. Mechanistic insights into the switch of αB-crystallin chaperone activity and self-multimerization. J. Biol. Chem. 293:14880–90
    [Google Scholar]
  75. 75. 
    Lu K, Psakhye I, Jentsch S 2014. Autophagic clearance of polyQ proteins mediated by ubiquitin-Atg8 adaptors of the conserved CUET protein family. Cell 158:549–63
    [Google Scholar]
  76. 76. 
    Mainz A, Peschek J, Stavropoulou M, Back KC, Bardiaux B et al. 2015. The chaperone αB-crystallin uses different interfaces to capture an amorphous and an amyloid client. Nat. Struct. Mol. Biol. 22:898–905
    [Google Scholar]
  77. 77. 
    Malinovska L, Kroschwald S, Munder MC, Richter D, Alberti S 2012. Molecular chaperones and stress-inducible protein-sorting factors coordinate the spatiotemporal distribution of protein aggregates. Mol. Biol. Cell 23:3041–56
    [Google Scholar]
  78. 78. 
    Marshall RS, McLoughlin F, Vierstra RD 2016. Autophagic turnover of inactive 26S proteasomes in yeast is directed by the ubiquitin receptor Cue5 and the Hsp42 chaperone. Cell Rep 16:1717–32
    [Google Scholar]
  79. 79. 
    McHaourab HS, Lin YL, Spiller BW 2012. Crystal structure of an activated variant of small heat shock protein Hsp16.5. Biochemistry 51:5105–12
    [Google Scholar]
  80. 80. 
    Miller SB, Ho CT, Winkler J, Khokhrina M, Neuner A et al. 2015. Compartment-specific aggregases direct distinct nuclear and cytoplasmic aggregate deposition. EMBO J 34:778–97
    [Google Scholar]
  81. 81. 
    Miller SB, Mogk A, Bukau B 2015. Spatially organized aggregation of misfolded proteins as cellular stress defense strategy. J. Mol. Biol. 427:1564–74
    [Google Scholar]
  82. 82. 
    Mogk A, Bukau B. 2017. Role of sHsps in organizing cytosolic protein aggregation and disaggregation. Cell Stress Chaperones 22:493–502
    [Google Scholar]
  83. 83. 
    Mogk A, Bukau B, Kampinga HH 2018. Cellular handling of protein aggregates by disaggregation machines. Mol. Cell 69:214–26
    [Google Scholar]
  84. 84. 
    Mogk A, Deuerling E, Vorderwulbecke S, Vierling E, Bukau B 2003. Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol. Microbiol. 50:585–95
    [Google Scholar]
  85. 85. 
    Mogk A, Schlieker C, Friedrich KL, Schönfeld H-J, Vierling E, Bukau B 2003. Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK. J. Biol. Chem. 278:31033–42
    [Google Scholar]
  86. 86. 
    Mok SA, Condello C, Freilich R, Gillies A, Arhar T et al. 2018. Mapping interactions with the chaperone network reveals factors that protect against tau aggregation. Nat. Struct. Mol. Biol. 25:384–93
    [Google Scholar]
  87. 87. 
    Morelli FF, Verbeek DS, Bertacchini J, Vinet J, Mediani L et al. 2017. Aberrant compartment formation by HSPB2 mislocalizes lamin A and compromises nuclear integrity and function. Cell Rep 20:2100–15
    [Google Scholar]
  88. 88. 
    Mymrikov EV, Daake M, Richter B, Haslbeck M, Buchner J 2017. The chaperone activity and substrate spectrum of human small heat shock proteins. J. Biol. Chem. 292:672–84
    [Google Scholar]
  89. 89. 
    Narberhaus F. 2002. α-Crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol. Mol. Biol. Rev. 66:64–93
    [Google Scholar]
  90. 90. 
    Narberhaus F, Waldminghaus T, Chowdhury S 2006. RNA thermometers. FEMS Microbiol. Rev. 30:3–16
    [Google Scholar]
  91. 91. 
    Nillegoda NB, Kirstein J, Szlachcic A, Berynskyy M, Stank A et al. 2015. Crucial HSP70 co-chaperone complex unlocks metazoan protein disaggregation. Nature 524:247–51
    [Google Scholar]
  92. 92. 
    Painter AJ, Jaya N, Basha E, Vierling E, Robinson CV, Benesch JL 2008. Real-time monitoring of protein complexes reveals their quaternary organization and dynamics. Chem. Biol. 15:246–53
    [Google Scholar]
  93. 93. 
    Peschek J, Braun N, Rohrberg J, Back KC, Kriehuber T et al. 2013. Regulated structural transitions unleash the chaperone activity of αB-crystallin. PNAS 110:E3780–89
    [Google Scholar]
  94. 94. 
    Peters LZ, Karmon O, David-Kadoch G, Hazan R, Yu T et al. 2015. The protein quality control machinery regulates its misassembled proteasome subunits. PLOS Genet 11:e1005178
    [Google Scholar]
  95. 95. 
    Plesofsky-Vig N, Brambl R. 1995. Disruption of the gene for hsp30, an α-crystallin-related heat shock protein of Neurosporacrassa, causes defects in thermotolerance. PNAS 92:5032–36
    [Google Scholar]
  96. 96. 
    Rajagopal P, Tse E, Borst AJ, Delbecq SP, Shi L et al. 2015. A conserved histidine modulates HSPB5 structure to trigger chaperone activity in response to stress-related acidosis. eLife 4:e07304
    [Google Scholar]
  97. 97. 
    Ratajczak E, Zietkiewicz S, Liberek K 2009. Distinct activities of Escherichia coli small heat shock proteins IbpA and IbpB promote efficient protein disaggregation. J. Mol. Biol. 386:178–89
    [Google Scholar]
  98. 98. 
    Saarikangas J, Barral Y. 2015. Protein aggregates are associated with replicative aging without compromising protein quality control. eLife 4:e06197
    [Google Scholar]
  99. 99. 
    Santhanagopalan I, Degiacomi MT, Shepherd DA, Hochberg GKA, Benesch JLP, Vierling E 2018. It takes a dimer to tango: Oligomeric small heat shock proteins dissociate to capture substrate. J. Biol. Chem. 293:19511–21
    [Google Scholar]
  100. 100. 
    Servant P, Mazodier P. 2001. Negative regulation of the heat shock response in Streptomyces. Arch. Microbiol 176:237–42
    [Google Scholar]
  101. 101. 
    Shi J, Koteiche HA, McDonald ET, Fox TL, Stewart PL, McHaourab HS 2013. Cryoelectron microscopy analysis of small heat shock protein 16.5 (Hsp16.5) complexes with T4 lysozyme reveals the structural basis of multimode binding. J. Biol. Chem. 288:4819–30
    [Google Scholar]
  102. 102. 
    Shiber A, Breuer W, Brandeis M, Ravid T 2013. Ubiquitin conjugation triggers misfolded protein sequestration into quality-control foci when Hsp70 chaperone levels are limiting. Mol. Biol. Cell 24:2076–87
    [Google Scholar]
  103. 103. 
    Sobott F, Benesch JL, Vierling E, Robinson CV 2002. Subunit exchange of multimeric protein complexes: real-time monitoring of subunit exchange between small heat shock proteins by using electrospray mass spectrometry. J. Biol. Chem. 277:38921–29
    [Google Scholar]
  104. 104. 
    Solis EJ, Pandey JP, Zheng X, Jin DX, Gupta PB et al. 2016. Defining the essential function of yeast Hsf1 reveals a compact transcriptional program for maintaining eukaryotic proteostasis. Mol. Cell 63:60–71
    [Google Scholar]
  105. 105. 
    Song J, Yang Q, Yang J, Larsson L, Hao X et al. 2014. Essential genetic interactors of SIR2 required for spatial sequestration and asymmetrical inheritance of protein aggregates. PLOS Genet 10:e1004539
    [Google Scholar]
  106. 106. 
    Specht S, Miller SB, Mogk A, Bukau B 2011. Hsp42 is required for sequestration of protein aggregates into deposition sites in Saccharomycescerevisiae. J. Cell Biol 195:617–29
    [Google Scholar]
  107. 107. 
    Spokoini R, Moldavski O, Nahmias Y, England JL, Schuldiner M, Kaganovich D 2012. Confinement to organelle-associated inclusion structures mediates asymmetric inheritance of aggregated protein in budding yeast. Cell Rep 2:738–47
    [Google Scholar]
  108. 108. 
    Stengel F, Baldwin AJ, Bush MF, Hilton GR, Lioe H et al. 2012. Dissecting heterogeneous molecular chaperone complexes using a mass spectrum deconvolution approach. Chem. Biol. 19:599–607
    [Google Scholar]
  109. 109. 
    Stengel F, Baldwin AJ, Painter AJ, Jaya N, Basha E et al. 2010. Quaternary dynamics and plasticity underlie small heat shock protein chaperone function. PNAS 107:2007–12
    [Google Scholar]
  110. 110. 
    Stromer T, Ehrnsperger M, Gaestel M, Buchner J 2003. Analysis of the interaction of small heat shock proteins with unfolding proteins. J. Biol. Chem. 278:18015–21
    [Google Scholar]
  111. 111. 
    Strozecka J, Chrusciel E, Gorna E, Szymanska A, Zietkiewicz S, Liberek K 2012. Importance of N- and C-terminal regions of IbpA, Escherichia coli small heat shock protein, for chaperone function and oligomerization. J. Biol. Chem. 287:2843–53
    [Google Scholar]
  112. 112. 
    Ungelenk S, Moayed F, Ho CT, Grousl T, Scharf A et al. 2016. Small heat shock proteins sequester misfolding proteins in near-native conformation for cellular protection and efficient refolding. Nat. Commun. 7:13673
    [Google Scholar]
  113. 113. 
    van Montfort R, Slingsby C, Vierling E 2001. Structure and function of small heat shock protein/α-crystallin family of molecular chaperones. Adv. Protein Chem. 59:105–56
    [Google Scholar]
  114. 114. 
    van Montfort RL, Basha E, Friedrich KL, Slingsby C, Vierling E 2001. Crystal structure and assembly of a eukaryotic small heat shock protein. Nat. Struct. Biol. 8:1025–30
    [Google Scholar]
  115. 115. 
    Veinger L, Diamant S, Buchner J, Goloubinoff P 1998. The small heat shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J. Biol. Chem. 273:11032–37
    [Google Scholar]
  116. 116. 
    Waldminghaus T, Gaubig LC, Klinkert B, Narberhaus F 2009. The Escherichia coli ibpA thermometer is comprised of stable and unstable structural elements. RNA Biol 6:455–63
    [Google Scholar]
  117. 117. 
    Walther DM, Kasturi P, Zheng M, Pinkert S, Vecchi G et al. 2015. Widespread proteome remodeling and aggregation in aging C.elegans. Cell 161:919–32
    [Google Scholar]
  118. 118. 
    Waters ER, Vierling E. 1999. The diversification of plant cytosolic small heat shock proteins preceded the divergence of mosses. Mol. Biol. Evol. 16:127–39
    [Google Scholar]
  119. 119. 
    Wolfe KJ, Ren HY, Trepte P, Cyr DM 2013. The Hsp70/90 cochaperone, Sti1, suppresses proteotoxicity by regulating spatial quality control of amyloid-like proteins. Mol. Biol. Cell 24:3588–602
    [Google Scholar]
  120. 120. 
    Zhou C, Slaughter BD, Unruh JR, Guo F, Yu Z et al. 2014. Organelle-based aggregation and retention of damaged proteins in asymmetrically dividing cells. Cell 159:530–42
    [Google Scholar]
  121. 121. 
    Zwirowski S, Klosowska A, Obuchowski I, Nillegoda NB, Pirog A et al. 2017. Hsp70 displaces small heat shock proteins from aggregates to initiate protein refolding. EMBO J 36:783–96
    [Google Scholar]
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